The Association of Hepatitis B Vaccine Supply Policy with Timing of Receipt of the First Dose of Hepatitis B Vaccination

doi:10.4236/ojs.2012.24053

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Open Journal of Statistics, 2012, 2, 429-434

http://dx.doi.org/10.4236/ojs.2012.24053 Published Online October 2012 (http://www.SciRP.org/journal/ojs)

The Association of Hepatitis B Vaccine Supply Policy with

Timing of Receipt of the First Dose of Hepatitis B

Vaccination

Zhen Zha o1, Trudy V. Murphy2

1National Center for Immunization and Respiratory Diseases, Centers for Disease Control and Prevention, Atlanta, USA

2National Center for HIV/AIDS, Viral Hepatitis, STD&TB Prevention, Centers for Disease Control and Prevention, Atlanta, USA

Email: [email protected]

Received July 11, 2012; revised August 14, 2012; accepted August 26, 2012

ABSTRACT

An estimated 800,000 - 1.4 million persons in the US have chronic Hepatitis B Virus (HBV) infection. The risk for

chronic infection is greatest among young children; approximately 90% of infants will remain chronically infected with

HBV. Approximately 25% of those who become chronically infected during childhood die prematurely from cirrhosis

or liver cancer. Hepatitis B vaccination is the most effective measure to prevent HBV infection and its consequences. In

2006, 29 US states had Hepatitis B Vaccine Supply (HBVS) policy which either supplies hepatitis B vaccine at no cost

to all providers for all children or provides hepatitis B vaccine to delivery hospitals-only free of charge for all infants;

other 21 US states and the District of Columbia did not have. 17,636 infants born in 2006 obtained from 2007-2009

National Immunization Survey (NIS) were analyzed with survival analysis procedures of Kaplan-Meier estimate and

Cox proportional hazards model for complex sample survey to evaluate the association between state HBVS policy and

the timing of infant age in days to receipt of hepatitis B vaccination. State HBVS policy is associated with infant age in

days from birth to receipt of the first dose of hepatitis B vaccine (P < 0.01), and to completion of the 3-dose hepatitis B

vaccine series (P < 0.01). Receipt of the first dose of hepatitis B vaccine occurred 31% earlier among infants residing in

states with HBVS policy than among infants residing in states without (adjusted hazards ratio 1.31, 95%CI (1.23, 1.39)).

Completion of the 3-dose hepatitis B vaccine series were 12% sooner among infants living in states with HBVS policy

than among infants living in states without (adjusted hazards ratio 1.12, 95%CI (1.06, 1.18)). State HBVS policy may

help overcome barriers to timely delivery of hepatitis B vaccines to infants.

Keywords: First Dose Hepatitis B Vaccine; 3-Dose Hepatitis B Vaccine Series; Vaccine Supply Policy; Vaccination

Coverage; Cox Proportional Hazards Model

1. Introduction

An estimated 800,000 - 1.4 million persons in the US

have chronic hepatitis B virus (HBV) infection. The risk

for chronic infection is greatest among young children;

approximately 90% of infants will remain chronically

infected with HBV. By contrast, about 95% of adults

recover completely from HBV infection and do not be-

come chronically infected. Approximately 25% of those

who become chronically infected during childhood die

prematurely from cirrhosis or liver cancer [1]. Hepatitis

B vaccination is the most effective measure to prevent

HBV infection and its consequences. Completion of

hepatitis B immunization alone, when started within the

first day of life, prevents 70% - 95% of perinatal HBV

infections, as well as early childhood HBV infections

acquired from HBV-infected household contacts [2]. In

1991, the Advisory Committee on Immunization Prac-

tices (ACIP) proposed, for the first time, that hepatitis B

vaccination be recommended for all infants regardless of

the hepatitis B surface antigen (HBsAg) status of the

mother [3]. The preferred vaccination schedule of the

ACIP and the American Academy of Pediatrics (AAP)

calls for administering the first dose of hepatitis B vac-

cine during the newborn period, before the infant is dis-

charged from the hospital; the second dose at age 1 to 2

months; and the third dose at age 6 to 18 months [3-5].

The critical feature of the recommendation is to initiate

the 3-dose hepatitis B vaccine series at birth.

In the US, a state vaccine financing policy describes

which groups of children and in which settings the state

will purchase vaccine with Vaccines for Children (VFC)

program funds, Public Health Service Section 317 Im-

munization Grants Program funds, or state funds. The

state vaccine financing policies range from very com-

Z. ZHAO, T. V. MURPHY

430

prehensive approaches, such as a Universal vaccine fi-

nancing policy, in which the state provides all vaccines

to all providers for all children, to approach in which the

state only provides vaccines for those children who are

VFC eligible [6,7].

The uptake of heptavalent pneumococcal conjugate

vaccine (PCV7) among children aged 19 to 35 months

residing in the United States and how uptake rates dif-

fered by state vaccine financing policy were evaluated

with logistic regression [7].

The research letter [8] suggested that the median of

hepatitis B birth dose vaccination rate might be higher

for infants with than without specific hospital hepatitis B

vaccine supply policy. The birth dose of hepatitis B vac-

cination status (yes vs. no) was defined as the first dose

of hepatitis B vaccine administered within 2 days of life

for infants born in 2002. Due to the data limitation, non-

parametric Wilcoxon rank-sum test was applied to com-

pare the median of hepatitis B birth dose vaccination

rates between the two independent groups. Thus that

analysis couldn’t account for the critical timing informa-

tion of infant age in days from birth to receipt of the first

dose of hepatitis B vaccine, and might compromise the

precision of the estimate and inference for the effect of

specific hospital hepatitis B vaccine supply policy. In

addition, the association of specific hospital hepatitis B

vaccine supply policy with completion of the 3-dose

hepatitis B vaccine series was not evaluated.

Robust data were lacking with regard to the associa-

tion between timing of infants age in days to receipt of

hepatitis B vaccination and state Hepatitis B Vaccine

Supply (HBVS) policy which will be defined in Section

2.2. In this study, we conducted a birth year cohort study

with infants born in 2006 obtained from 2007-2009 Na-

tional Immunization Survey (NIS). The primary objec-

tive of this study is to evaluate the association of state

HBVS policy with timing of infant age in days from birth

to receipt of the first dose of hepatitis B vaccine. The

secondary objective is to assess whether state HBVS

policy is associated with earlier completion of the 3-dose

hepatitis B vaccine series. In order to achieve the above

two objectives, survival analysis for complex sample

survey data was applied in this study.

2. Materials and Methods

2.1. Data Resource

A cohort of infants born in 2006 in the US was analyzed

in this study. Information about this birth cohort was

obtained from NIS conducted during 2007-2009. The

NIS is carried out annually by the Centers for Disease

Control and Prevention (CDC) to acquire national, state,

and selected urban-area estimates of vaccination cover-

age for the US non-institutionalized population of chil-

dren age 19 - 35 months [9]. For NIS 2007-2009 data, the

overall household response rates based on Council of

American Survey and Research Organizations (CASRO)

guidelines ranged from 63.2% to 64.9% [10]. The analy-

ses in this study were limited to children with adequate

provider data, children for whom sufficient vaccination

history information is obtained from their providers to

determine whether they are up-to-date with respect to the

recommended vaccination schedule, the proportions of

children with adequate provider data ranged from 85.4%

to 87.6% [10]. In the 2006 birth cohort, there were

17,636 infants that represented approximate 4.3 million

infants born in the US in 2006.

The socio-demographic factors related to infants, fam-

ily, mother, and vaccination provider available in the NIS

were examined in both univariate and multivariable

analyses. Those factors have previously been found to be

associated with infant vaccination coverage in the United

States [11-13]: infant race/ethnicity (Non-Hispanic White,

Non-Hispanic Black, Hispanic, other), first born status

(yes vs. no), and number of siblings (0 vs. ≥1); family

poverty status (at or above vs. below poverty level), and

locality (urban, suburban, rural); mother’s education level

(≤12 years vs. >12 years), marital status (married vs. not

married), and mother’s age (≤29 years vs. ≥30 years);

number (1 vs. ≥2) and type (public, private, other) of

vaccination providers; and survey interview language

(English, Spanish, or other).

2.2. State Hepatitis B Vaccine Supply (HBVS)

Policy

In the US, a state vaccine financing policy was self-re-

ported by the state immunization program to the National

Center for Immunization and Respiratory Diseases, Cen-

ters for Disease Control and Prevention. The states were

defined by their vaccine financing policy category: Uni-

versal; Universal-Select; VFC and Underinsured; VFC

and Underinsured-Select; VFC-Only; and Other [6,7,14].

The states with Universal or Universal-Select policy

supply hepatitis B vaccine among others at no cost to all

vaccination providers for all children, in 2006 sixteen

states were in this category (Alaska, New Hampshire,

New Mexico, Rhode Island, Vermont, Washington, Con-

necticut, Hawaii, Idaho, Maine, Massachusetts, Nevada,

North Carolina, North Dakota, South Dakota, and Wyo-

ming). In addition, some states have established a spe-

cific hospital hepatitis B vaccine supply policy that pro-

vides hepatitis B vaccine to delivery hospitals-only free

of charge for all infants regardless of the eligibility for

VFC or the health insurance status of infants [8]. In 2006,

thirteen states were in this category (Arizona, Arkansas,

Kansas, Kentucky, Louisiana, Michigan, Montana, New

York, Ohio, Oregon, Pennsylvania, Utah, and Wisconsin).

Z. ZHAO, T. V. MURPHY 431

Data on state specific hospital hepatitis B vaccine supply

policy were obtained from CDC’s Perinatal Hepatitis B

Prevention Program Annual Assessment Report for year

2006; this is the most recent information available on

state specific hospital hepatitis B vaccine supply policy.

To explore the association of hepatitis B vaccine sup-

ply policy with infant hepatitis B vaccination, in this

study, the preceding two types of policies together are

defined as state Hepatitis B Vaccine Supply (HBVS)

policy. Thus, in 2006 in the US, 29 US states had state

HBVS policy; and 21 US states and the District of Co-

lumbia did not have state HBVS policy.

2.3. Statistical Analyses

Survival analysis procedures for complex sample survey

[15] were adopted to evaluate the association of state

HBVS policy defined above with timing of infant hepati-

tis B vaccination. In the primary analysis, the “time” de-

pendent variable was defined as infant age in days from

birth to receipt of the first dose of hepatitis B vaccine.

The unprecedented feature of the recommended hepatitis

B vaccination schedule by ACIP and AAP is to initiate

hepatitis B vaccine series at birth, thus in this study if

infant age in days from birth to the first dose of hepatitis

B vaccination was less than or equal to 30 days then this

age was defined as an event, otherwise the age was right

censored at 30 days [5,16]. As for completion of the

3-dose hepatitis B vaccine series, by the recommended

schedule the third dose of hepatitis B vaccine should be

administered at least 112 days (16 weeks) after the first

dose and completed by 549 days (18 months) of age.

Thus in the secondary analysis, infants whose age being

greater than or equal to 112 days were included, and if

infant age in days from birth to the third dose of hepatitis

B vaccination was less than or equal to 549 days, then

the age was defined as an event, otherwise the age was

right censored at 549 days.

The two cumulative vaccination coverage curves for

the first dose of hepatitis B vaccination were estimated

with the use of Kaplan-Meier model by infant age in

days and stratified by state HBVS policy status (yes vs.

no), and were compared with the use of log-rank test.

Similarly, the cumulative vaccination coverage curve

estimation and comparison for completion of the 3-dose

hepatitis B vaccine series applied. The Cox proportional

hazards model [17,18] was applied to evaluate the asso-

ciation of state HBVS policy with infant age in days

from birth to receipt of the first dose of hepatitis B vac-

cine, also to completion of the 3-dose hepatitis B vaccine

series, controlling for the selected socio-demographic

factors. The backward-selection method [19,20] was ap-

plied to obtain the final model which contains the sig-

nificant predictors. The proportional hazards assumptions

of Cox model for NIS 2006 birth cohort data were ex-

amined by the graphic method, and were found to be

valid for all factors investigated.

3. Results

3.1. Prevalence Rates of State HBVS Policy

The prevalence rates of state HBVS policy across all

strata of the significant socio-demographic factors, which

were obtained in the final Cox model for evaluating the

association of state HBVS policy with infant age in days

from birth to receipt of the first dose of hepatitis B vac-

cine controlling for the selected socio-demographic fac-

tors, ranged from 26.9% to 46.9%, and the national rate

was 38.8%, as presented in Tab le 1. The prevalence rate

for Non-Hispanic White infants, 46.9%, was the highest

among all segments of race/ethnicity factor, and it was

significantly higher (p < 0.05) than the prevalence rate

for Non-Hispanic Black infants. The prevalence rate for

Hispanic infants, 26.9%, was the lowest (p < 0.05)

among all groups in race/ethnicity factor. Factor race/

ethnicity was significantly associated with state HBVS

policy status (p < 0.01). Infants whose mother’s educa-

tion >12 years were more likely than those whose

mother’s education ≤12 years to be residing in states

with HBVS policy (p < 0.01). Infants who had 1 vacci-

nation provider were more likely than those with ≥2

vaccination providers to live in HBVS policy states (p =

0.02).

3.2. The Association of State HBVS Policy with

the First Dose of Hepatitis B Vaccination

Two curves for the first dose of hepatitis B cumulative

vaccination coverage by infant age in days stratified by

state HBVS policy status were shown in Figure 1. Over-

all, the cumulative vaccination coverage for the first dose

of hepatitis B vaccine was significantly higher for infants

living in states with HBVS policy than infants living in

states without such policy (p-value < 0.01 by the log-

rank test). Table 2 presented the hepatitis B first dose

cumulative vaccination coverage with 95% confidence

interval at infant age 0 through 3 days, and 1 through 4

weeks for all infants and stratified by state HBVS policy

status. At each specific infant age, infants residing in

states with HBVS policy would be most likely (p-value <

0.05) to receive the first dose of hepatitis B vaccine

compared to infants residing in states without such pol-

icy.

The main effect of state HBVS policy was signifi-

cantly associated with infant age in days from birth to

receipt of the first dose of hepatitis B vaccine (p-value <

0.01, F-test) controlling for the six significant covariates

acquired from the Cox model. Receipt of the first dose of

hepatitis B vaccine occurred significantly earlier among

infants living in states with HBVS policy than among

Z. ZHAO, T. V. MURPHY

432

Table 1. Prevalence rates of state Hepatitis B Vaccine Sup-

ply (HBVS) policy by selected socio-demogr aphic fact or s.

Factor N Weighted % (95%CI)p-value

Total 17,636 38.8 (38.1, 39.5)

Race/ethnicity of infant

Non-Hispanic white 10,886 46.9 (45.7, 48.2)

Non-Hispanic black 1785 32.5 (29.3, 35.7)

Hispanic 3281 26.9 (24.9, 29.0)

Other 1684 39.1 (35.4, 42.9)

<0.01

Mother’s education

≤12 years 5208 36.8 (35.1, 38.5)

>12 years 12,428 40.9 (40.0, 41.9)

<0.01

Type of vaccination

provider

Private 11,207 38.3 (37.2, 39.4)

Public 1896 37.1 (33.7, 40.6)

Other 4372 40.9 (38.4, 43.3)

0.20

Number of

vaccination providers

1 12,118 39.8 (38.73, 40.92)

≥2 5485 36.8 (34.86, 38.69)

0.02

First born status

of infant

No 9330 37.8 (36.4, 39.1)

Yes 8306 40.0 (38.6, 41.5)

0.07

Mother’s age

≤29 years 6198 38.8 (37.0, 40.7)

≥30 years 11,438 38.8 (37.7, 39.9)

0.98

80%

70%

60%

50%

40%

30%

20% 0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30

Age in days

HBVS Policy = YesHBVS Policy = No

Figure 1. Cumulative vaccination coverage in percentage

for the first dose of Hepatitis B (HepB) vaccine by infant

age in days stratified by state Hepatitis B Vaccine Supply

(HBVS) policy status.

Table 2. Cumulative vaccination coverage for the first dose

of Hepatitis B (HepB) vaccine by infant age in days/weeks

stratified by state Hepatitis B Vaccine Supply (HBVS) pol-

icy status.

Infant

Age

All Infants

%(95%CI)

HBVS Policy = Yes

%(95%CI)

HBVS Policy = No

%(95%CI)

0 day34.5 (33.3, 35.8)37.4 (35.8, 39.0) 32.7 (30.9, 34.5)

1 day50.6 (49.3, 51.9)56.3 (54.7, 57.9) 47.0 (45.1, 48.9)

2 days57.2 (55.9, 58.5)64.4 (62.8, 65.9) 52.7 (50.8, 54.6)

3 days58.7 (57.4, 60.0)65.8 (64.3, 67.4) 54.2 (52.3, 56.1)

1 week61.9 (60.6, 63.2)68.9 (67.4, 70.3) 57.5 (55.7, 59.4)

2 weeks64.5 (63.2, 65.8)70.9 (69.4, 72.3) 60.4 (58.6, 62.3)

3 weeks65.9 (64.6, 67.1)71.8 (70.3, 73.2) 62.1 (60.3, 64.0)

4 weeks66.7 (65.4, 67.9)72.3 (70.8, 73.7) 63.2 (61.3, 65.0)

infants living in states without such policy (adjusted haz-

ards ratio 1.31, 95%CI (1.23, 1.39)); significantly earlier

among Non-Hispanic Black infants than among Non-

Hispanic White infants (adjusted hazards ratio 1.16,

95%CI (1.04, 1.29)); and significantly sooner among

infants having multiple vaccination providers than among

infants having only 1 vaccination provider (adjusted haz-

ards ratio 1.25, 95%CI (1.17, 1.35)) as presented in Ta-

ble 3. In addition, the result acquired by unadjusted Cox

model were consistent with the result obtained from the

adjusted Cox model with regard to the significance status

of state HBVS policy measured by hazards ratios.

3.3. The Association between Completion of the

3-Dose Hepatitis B Vaccine Series and State

HBVS Policy

The two cumulative vaccination coverage curves for

completion of the 3-dose hepatitis B vaccine series by

infant age in days stratified by state HBVS policy status

were estimated and compared. In general, the cumulative

vaccination coverage for completion of the 3-dose hepa-

titis B vaccine series was significantly higher among

infants living in states with HBVS policy than among

infants living in states without such policy (p-value <

0.01 by the log-rank test).

The main effect of state HBVS policy was signifi-

cantly associated with infant age in days from birth to

completion of the 3-dose hepatitis B vaccine series

(p-value < 0.01, F-test) controlling for other six signifi-

cant predictors obtained from the Cox model. The adjusted

hazards ratio for state HBVS policy 1.12, with 95%CI (1.06,

1.18), suggested that completion of the 3-dose hepatitis B

vaccine series was significantly sooner among infants

residing in states with HBVS policy than among infants

residing in states without such policy. Infants who

Z. ZHAO, T. V. MURPHY 433

Table 3. Hazards Ratio (HR) of infant age in days from

birth to receipt of the first dose of hepatitis B vaccine be-

tween strata of state Hepatitis B Vaccine Supply (HBVS)

policy and the significant socio-demographic factors.

Factors

Unadjusted

(95%CI)

Multivariable

Adjusted HR

(95%CI)

State Hepatitis B Vaccine Supply

(HBVS) policy status

Yes 1.28

(1.20, 1.36)

1.31

(1.23, 1.39)

No 1.00 1.00

Race/ethnicity of infant

Non-Hispanic white 1.00 1.00

Non-Hispanic black 1.14

(1.02, 1.26)

1.16

(1.04, 1.29)

Hispanic 1.09

(1.00, 1.18)

1.09

(1.00, 1.19)

Other 1.15

(1.03, 1.29)

1.17

(1.05, 1.30)

Mother’s education

≤12 years 1.13

(1.06, 1.21)

1.08

(1.01, 1.16)

>12 years 1.00 1.00

Type of vaccination providers

Private 1.01

(0.89, 1.13)

1.09

(0.96, 1.23)

Public 1.00 1.00

Other 1.19

(1.05, 1.36)

1.16

(1.02, 1.32)

Number of vaccination providers

1 1.00 1.00

≥2 1.29

(1.20, 1.38)

1.25

(1.17, 1.35)

First born status of infant

No 1.00 1.00

Yes 0.96

(0.90, 1.03)

0.94

(0.88, 1.00)

Mother’s age

≤29 years 1.16

(1.08, 1.24)

1.11

(1.03, 1.19)

≥30 years 1.00 1.00

had 0 sibling were significantly earlier than infants who

had 1 or more siblings with respect to completion of the

3-dose hepatitis B vaccine series (adjusted hazards ratio

1.13, 95%CI (1.06, 1.21)). Also, the significance status

of state HBVS policy gained by unadjusted Cox model,

(hazards ratio 1.11, 95%CI (1.05, 1.17)), was consistent

with the result achieved from the adjusted Cox model,

(hazards ratio 1.12, 95%CI (1.06, 1.18)).

4. Discussion

In our current study, both the unadjusted and adjusted

analyses showed the consistent conclusions: infant age in

days from birth to receipt of the first dose of hepatitis B

vaccine was significantly associated with state HBVS

supply policy, hazards ratios are 1.28 (1.20, 1.36) and

1.31 (1.23, 1.39) respectively. Similarly, consistent and

significant results were obtained with regard to the asso-

ciation between infant age in days from birth to comple-

tion of the 3-dose hepatitis B vaccine series and state

HBVS policy, hazards ratios are 1.11 (1.05, 1.17) and

1.12 (1.06, 1.18) for unadjusted and adjusted analysis

separately. These consistent results suggested that the

association between hepatitis B vaccination and state

HBVS policy is both positive and robust.

This study suggested that state HBVS policy was sig-

nificantly associated with infant age in days from birth to

receipt of the first dose of hepatitis B vaccine. Infants

residing in states with HBVS policy received the first

dose of hepatitis B vaccine significantly early than those

residing in states without such policy. For example,

56.3% of infants with state HBVS policy received the

first dose of hepatitis B vaccine by age 1 day; however

56.0% of infants without state HBVS policy received the

first dose of hepatitis B vaccine by age 5 days. Similarly,

infants completed the 3-dose of hepatitis B vaccine series

significantly sooner among infants with state HBVS pol-

icy than among infants without such policy. For instance,

82.8% of infants with state HBVS policy completed the

3-dose hepatitis B vaccine series by age 10 months; but

82.8% of infants without such policy completed the

3-dose hepatitis B vaccine series by age 11.3 months.

This study showed that the first dose of hepatitis B

vaccine was administered significantly earlier among

infants residing in states with HBVS policy, which is

important. However, it is also important to know if state

HBVS policy is associated with earlier completion of the

3-dose hepatitis B vaccine series. As the secondary ob-

jective, this study suggested that state HBVS policy is

associated with earlier completion of the 3-dose hepatitis

B vaccine series. The significant and positive answer

strengthens the argument for state HBVS supply policy.

Some potential limitations of this study were that the

NIS used the random-digit-dial residential landline tele-

phone survey and has experienced under-representation

due to non-response and wireless telephone use. Al-

though the survey has been adjusted to account for these

changes, under-representation of households could in-

crease the potential bias in survey estimates. Also, non-

response bias after weighting adjustments and possible

incomplete ascertainment of hepatitis B vaccination by

provider record check may cause additional bias. Finally,

a few sub-state estimation areas rotated in or out in the

survey design during the last few years. However a re-

cent study [21] suggested that the total survey error in the

NIS may be small with a mean of 1.7%, 95%CI (1.71%,

Z. ZHAO, T. V. MURPHY

434

1.74%), and would likely not have changed the conclu-

sions in this study.

5. Conclusion

State HBVS policy has significantly improved access to

hepatitis B vaccine for infants in the US. This policy re-

sults in earlier first dose of hepatitis B vaccination, such

as before discharge from the delivery hospital or birthing

center, sooner completion of the 3-dose hepatitis B vac-

cine series, and higher hepatitis B vaccination coverage.

State HBVS policy may help overcome barriers to timely

delivery of hepatitis B vaccines to infants.

6. Disclaimer

The findings and conclusions in this article are solely the

responsibility of the authors and do not necessarily rep-

resent the official views of Centers for Disease Control

and Prevention.

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