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Correlates of Vaccination for Hepatitis B Among Adolescents
Results From a Parent Survey
Michael Seid, PhD;
Diana R. Simmes, MPH;
Leslie S. Linton, JD, MPH;
Christine E. Leah, MPH;
Christine C. Edwards, MPH;
K. Michael Peddecord, DrPH
Arch Pediatr Adolesc Med. 2001;155:921-926.
ABSTRACT
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Objective To identify correlates of hepatitis B vaccination status in sixth-grade
students in the year prior to implementation of a requirement mandating immunization
for seventh-grade entry.
Methods A survey of parents of sixth-graders in 5 schools in San Diego County.
Two logistic regression models were tested to predict the outcome variables:
initiation and completion of the vaccination series.
Results Factors associated with initiating the series included a recent nonacute
medical visit, white race, hearing about the vaccination law from a health
care provider, and the availability of a school-based vaccination clinic.
Factors associated with completing the series included English as the primary
language spoken at home, hearing about the law from a health care provider,
a school-based vaccination clinic, and higher socioeconomic status. Health
insurance was not significantly related to either outcome.
Conclusions There was a clear benefit for hepatitis B immunization status to have
had a recent nonacute medical visit, to have heard about the law from a health
care provider, and to have a school-based vaccination clinic. The factors
associated with starting vs completing the vaccination series were not identical.
However, both health care provider and school characteristics were related
to starting and completing the vaccination series. Thus, a multifaceted strategy
may be most appropriate for successful coverage of an adolescent population
with a vaccination series such as hepatitis B.
INTRODUCTION
HEPATITIS B is one of the most prevalent infectious diseases in the
world, with more than 300 million carriers of the virus worldwide.1 Estimates suggest that between 100 000 to 300 000
new cases of hepatitis B occur in the United States each year.2, 3, 4
In the United States, 63% of acute infections of hepatitis B occur in the
older adolescent or young adult population5, 6
(although prevalence is lower for younger adolescents than for older adolescents
and young adults) and most persons infected with hepatitis B acquired their
infection as adults or adolescents.7 This high
prevalence rate is especially disturbing given the existence of a readily
available effective vaccine. Adolescents are at a potentially increased risk
to the degree that they begin to experiment with high-risk behaviors such
as injection drug use, unprotected sex, tattooing, and body piercing.
In 1995, the Advisory Committee on Immunization Practices recommended
hepatitis B vaccinations for all 11- to 12-year-old children.8
Despite the recommendations, adolescent coverage rates have remained low.
For example, a population-based sample of parents of students planning to
enter fifth and sixth grade in San Diego County (California) in the fall of
1998 found that only 16% had completed the hepatitis B series.9
Immunization against hepatitis B is a 3-dose regimen and for "older children
and adolescents, doses may be given in a schedule of 0, 1, and 6 months or
of 0, 2, and 4 months."10
In 1997, the California state legislature passed AB 381, requiring proof
of hepatitis B immunization for all students entering, advancing to, transferring
into, and/or repeating the seventh grade on or after July 1, 1999.11 This law and the accompanying regulations follow
the current adolescent immunization recommendations approved by the Advisory
Committee on Immunization Practices, the American Academy of Pediatrics, and
the American Academy of Family Practitioners as condensed in the 1998 Schedule
published by the Centers for Disease Control and Prevention (Atlanta, Ga).12 The law permits that a child will be conditionally
admitted to school if he or she is currently up-to-date with the series. Parents
may claim a medical or personal belief exemption. Twenty other states (including
the District of Columbia) have had some form of middle school hepatitis B
vaccination law in effect since the end of 2000, with an additional 5 states
having laws that will go into effect in 2001 or later.13
With many other states considering such legislation, information about the
California experience will be relevant to health care providers and to state
and federal policy makers.
AB 381 is largely an unfunded mandate, providing only limited funds
to schools to check immunization records. With few additional resources made
available, effectiveness is crucial in immunizing the target population. What
roles should the provider and school communities play in implementing this
mandate? Pediatricians and family practitioners will likely be active participants
in any new vaccination requirement. As such, information about factors related
to immunization status will enable the health care provider community to maximize
the effectiveness of its response to laws such as those of California.
To organize the myriad of factors that might influence immunization
coverage, we used the widely accepted conceptual model, first proposed by
Donabedian,14 of structure, process, and outcome.
This model views health and health care as the outcomes of a production system
with both structural and process components.15
Structure refers to those factors necessary for health care services to occur,
such as adequate facilities and licensure of physicians, and to characteristics
of the patient population, such as sociodemographic variables or severity
of illness. In this study, we considered variables such as the presence of
a school-based vaccination clinic as well as insurance status, percentage
of the school population eligible for free and reduced-price lunch, race,
and primary language spoken at home to be structure variables. Process refers
to interactions within the health services system. We considered factors over
which providers have some control, such as the recency of the last nonacute
medical visit and whether the parent had heard about the immunization requirements
from a physician, clinic, or health plan, to be process variables. Outcomes
were the results of structure and process variables, specifically, the parents'
report of their child's immunization status.
PARTICIPANTS AND METHODS
OVERVIEW
A voluntary, anonymous survey for parents was conducted at 5 middle
schools participating in an ongoing examination of the effects of a seventh-grade
hepatitis B vaccination school entry requirement. The research protocol and
informed consent were reviewed and approved by the institutional review board
at San Diego State University.
PARTICIPATING SCHOOLS
We identified and selected 5 middle schools to participate in the survey.
Our criteria in assembling this group of schools were the following: (1) Schools
that planned to conduct on-site immunization clinics and schools that did
not plan such clinics. (2) Schools within the City of San Diego Unified School
District and in other districts. (3) Student populations generally representative
of the county (race and socioeconomic diversity [based on the percentage of
students eligible for federal free/reduced lunch programs]). (4) School staff
able to devote the time and effort necessary to administer and collect surveys.
Project staff interviewed a total of 11 schools and 5 schools met our criteria
and agreed to participate. These 5 included 3 schools in the San Diego Unified
School District, all of which had on-campus vaccination programs, and 2 outside
of the city school district, neither of which planned to have on-campus vaccination
programs. The 2 schools from outside the city school district were from 1
suburban and 1 rural district. The 5 schools had varied racial and socioeconomic
demographics as presented in Table 1.
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Table 1. Selected School Demographics and Response Rates*
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PROCEDURES
The survey was distributed to every sixth-grade student at each of the
5 schools during November 1998. Data used in this analysis were collected
from English-language surveys. Although a Spanish-language survey was fielded,
an error in translation resulted in omission of the main outcome variable.
Thus, the surveys from the 60 Spanish-speaking respondents were dropped from
the analysis. A project staff member or the classroom teacher handed out the
surveys during home room or "core" class time. Students were asked to take
the survey home, have a parent complete it, and return it to the classroom
teacher by the end of the week. Brightly colored baskets with signs reading
"Return Surveys Here" were placed in prominent locations in each classroom.
An incentive was offered to both the students and the teachers in an effort
to increase the response rate for returned surveys. All students were given
a thank-you item regardless of whether they had returned a survey. Teachers
received $1 for each completed and returned survey, with the money being used
to benefit classroom activities.
MEASURES
Schools were categorized based on the presence of a school-based vaccination
clinic. Three of the 5 schools had such a clinic prior to or during the survey
period. Schools were further categorized into higher vs lower socioeconomic
status, based on the percentage of the student body eligible for free or reduced-price
lunch. Because the percentage eligible ranged from 25% to 65%, the median
percentage of students eligible from the 5 schools (45.1%) was used to split
the sample. This resulted in 2 "lower SES [socioeconomic status]" schools
(percentage eligible greater than the median of the 5 schools) and 3 "higher
SES" schools (percentage eligible less than or equal to the median of the
5 schools). Higher SES was a relative term since in this category of schools,
25%, 38.7%, and 45.1% of the students were eligible for free and reduced-price
federal lunch programs.
Respondents were categorized based on primary language spoken at home
(English vs other), race (white vs other), and insurance status (any health
insurance vs none). Additionally, respondents were categorized based on whether
they reported having heard about the hepatitis B vaccination requirement from
their physician, clinic, or health plan (yes vs no) and on the recency of
nonacute medical visits (within the last 6 months vs 6-12 months ago vs more
than 1 year ago).
The outcome variable of hepatitis B vaccination status was based on
parents' recall of their child's immunization status. This variable was categorized
as no vaccinations, started the vaccination series (1 or 2 vaccinations),
and completed the vaccination series.
Additional data to assess potential bias were gathered from existing
data. The race distribution of the student body at each school was based on
data reported to the state.
ANALYSIS
The data were analyzed using SPSS version 8.0 (SPSS Inc, Chicago, Il).
Logistic regression was used to assess the effect of structure and process
variables on the main outcome: parent-reported adolescent hepatitis B immunization
status. Structure variables—both school factors (school-based vaccination
clinics, percentage of students eligible for free lunch) and personal factors
(primary language spoken at home, insurance status, race)—were entered
simultaneously as the first step (first block) in the regression equation.
Process variables (recency of last medical visit, whether parents had heard
about the law from a physician, clinic, or health plan) were entered simultaneously
as the second step (second block). All variables were forced to stay in the
model, using the ENTER option in SPSS. Two separate logistic regression equations
were constructed: 1 to predict beginning the vaccination series (any vaccinations
vs no vaccinations reported), and 1 to predict completing the vaccination
series (all vaccinations completed vs not all vaccinations completed). Recognizing
the possibility of a clustering effect that would cause the responses within
schools to be correlated, we also modeled school as a random effect in SAS
Proc Glimmix (SAS Institute, Cary, NC).16 The
quasi-likelihood estimates of the covariance parameters associated with school
were 0, so we reported the odds ratios (ORs) based on fixed effects only.
We report the  2 for each step of the regression equation,
the OR, and the confidence interval (CI) for the OR for each predictor.
RESULTS
A total of 1322 surveys were distributed at the 5 schools. Eight hundred
were returned, yielding an overall response rate of 60.5%. School response
rates ranged from a low of 46% to a high of 65%. Of the 800 returned surveys,
156 (19.5%) had missing data on at least one of the variables in the regression
equation, resulting in their being dropped from the regression analysis. We
examined these 2 potential threats to internal validity.
We examined the issue of nonresponse bias by comparing the sample with
available data on race and immunization status. We compared the race distribution
of the sample with that of the overall student body at each of the 5 participating
schools. Overall, the sample was fairly representative of the racial makeup
of the schools, with the exception of Latino students, who were underrepresented
by more than 10% in 3 of the 5 schools (Table 1). We compared immunization status of the sample with the
overall student body for 3 of the 5 schools from which data were available.
The overall sample showed 31% of students having no vaccinations, 39% having
1 or 2 vaccinations, and 29% having all 3 vaccinations. The data from the
schools showed that for the entire sixth grade, the respective percentages
were 47%, 30%, and 23%.
We examined the issue of bias owing to missing data by comparing the
analysis sample with those dropped because of missing data. The respondents
not included in the logistic regression analysis because of missing data were
more likely to attend a school with an on-campus vaccination program (82.8%
vs 70.5%; 21 = 7.5, P
= .006) and to be from a lower SES school (56.4% vs 42.4%; 21 = 10.0, P = .002). They were less likely
to speak English as the primary language at home (53.2% vs 76.9%; 21 35.1, P<.001), to be white
(22.2% vs 47.4%; 21 = 27.1, P<.001), to have health insurance (78.0% vs 89.4%; 21 13.0, P<.001), and to report hearing about
the hepatitis B law from their health care provider (16.7% vs 29.0%; 21 9.8; P = .002). There was no
difference between the included and excluded cases in the proportion with
a nonacute medical visit in the past 6 months (Table 2).
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Table 2. Sample Characteristics
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Descriptive data were reported based on the entire sample. As can be
seen, the overall sample is diverse, likely to be insured, and to speak English
as the primary language. Almost three quarters attended schools with a school-based
vaccination program, and the sample is equally split into higher and lower
SES schools. A little more than one third of the overall sample had been to
their health care provider for a nonacute visit in the past 6 months and about
one quarter reported that they had heard about the hepatitis B vaccination
requirement from a health care provider.
When asked whether their children had received any hepatitis B vaccinations
(n = 800), 29.1% of parents reported that their child had not been vaccinated,
2.5% reported that their child had received 1 or more vaccinations but were
not sure of the exact number, 16.1% reported that their child had received
the first vaccination, 17.9% reported 2 vaccinations, and 27.0% reported all
3 vaccinations (7.4% were missing or not sure). Of the parents who reported
that their child still needed 1 or more vaccinations (n = 679), the most common
reasons given for their child still needing vaccinations were not knowing
that their child needed vaccinations (20%), vaccinations were not yet medically
due (19%), and other (18%). The "other" category included a range of reasons,
including "against personal beliefs," "waiting for the school to give it to
him," and "procrastination."
The overall percentage of parents (n = 679) reporting that their child
had health care coverage of some type is similar to the 85% reported in San
Diego County overall.17 Those speaking primarily
English at home were more likely to report that they had health insurance
(91%) than those who reported speaking primarily another language at home
(73%) (21 = 49.8; P<.001).
Those with health insurance were more likely to report that their child had
received a regular medical checkup in the last 6 months when compared with
those without insurance (39% and 22% respectively; 21 = 15.4; P<.001).
Three of the 5 schools in the sample administered vaccinations on campus.
Children attending these 3 schools were more likely than those at schools
not offering vaccinations to be nonwhite (63.7% vs 44.3%; 21 = 24.6; P<.001), to primarily speak a
language other than English at home (31.0% vs 19.2%; 21 = 11.1; P<.001), and to be a student at
a higher SES school (61.6% vs 37.0%; 21 = 39.0; P<.001).
Two logistic regression models were generated, one to identify factors
associated with an increased likelihood of having started the vaccination
series (Table 3) and one to identify
factors associated with an increased likelihood of having completed the vaccination
series (Table 4).
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Table 3. Logistic Regression Analysis Predicting Starting the Hepatitis
B Vaccination Series*
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Table 4. Logistic Regression Analysis Predicting Completing the Hepatitis
B Vaccination Series
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In the regression model predicting those who started the vaccination
series (n = 644), the largest OR was related to having had a nonacute medical
visit in the last 6 months (OR, 2.2; 95% CI, 1.39-3.51 compared with a visit
6-12 months ago; OR, 3.36; 95% CI, 2.18-5.16 compared with a visit more than
a year ago). Other significant predictors were white race (OR, 1.96; 95% CI,
1.27-3.00), attending a school with an on-campus vaccination program (OR,
1.56; 95% CI, 1.04-2.34), and having heard about the law from a health care
provider (OR, 1.74; 95% CI, 1.14-2.65).
In the regression model predicting those who completed the vaccination
series (n = 644), significant ORs were associated with attending a school
with a vaccination program (OR, 1.80; 95% CI, 1.15-2.80), attending a higher
SES school (OR, 1.52; 95% CI, 1.00-2.30), primarily speaking English at home
(OR, 2.22; 95% CI, 1.38-3.57), and having heard about the law from a health
care provider (OR, 1.81; 95% CI, 1.23-2.65). Health insurance status was not
significantly related to either of the outcomes measured.
COMMENT
This study examined the correlates of adolescent hepatitis B vaccination
coverage in the year prior to an impending vaccination mandate. Two factors
emerged as significant in starting and in completing the vaccination series:
attending a school with an on-campus vaccination clinic and having heard about
the law from a health care provider (eg, a physician, clinic, or health plan).
The factor found to be the strongest determinant of starting the series—a
well-child visit in the last 6 months—did not predict completion of
the series. This may be because many adolescents had started their series
at a physician's office but had not yet returned to complete the series. Surprisingly,
our analysis showed that health insurance status, a traditional measure of
access, was not directly related to the outcomes of interest and may therefore
be less important than health services–seeking behavior (eg, recent
health care visit) in immunization coverage.
These findings highlight the roles of health care providers and of schools
in raising hepatitis B coverage rates. Provider behavior was related to increased
coverage rates in that having heard about the new vaccination requirement
from a physician, clinic, or health plan was a consistent predictor of both
starting and finishing the vaccination series. This finding suggests the crucial
importance of efforts on the part of the health care provider community to
educate parents and patients. The benefit of having a recent nonacute medical
visit is clear in terms of starting the hepatitis B series. Follow-up of this
cohort might have revealed a benefit of a recent nonacute medical visit in
terms of completing the series.
Because more than 99% of children attend school until at least age 13
years,18 school-based vaccination campaigns
would seem to be an important part of an effective strategy for reaching large
numbers of young adolescents. Previous studies have indicated that school-based
vaccination programs can efficiently provide vaccination services19 and that most parents are accepting of such programs.19, 20 Our findings support this idea.
These findings have policy implications for other states considering
implementation of a law such as AB 381. That different determinants emerged
for starting vs finishing the vaccination series implies that a multifaceted
approach may be necessary for successful coverage of an adolescent population
with a vaccination series such as hepatitis B. Given the potential costs associated
with such an initiative, state policy makers may see tension between the health
care provider and school communities in the implementation of this mandate.
Our findings suggest, however, that both providers and schools must play active
roles in the implementation. In this sample, there was a clear benefit to
immunization status both in being a student where school-based vaccination
clinics were held, as well as in having heard about the law from a health
care provider and having had a recent health care visit. The fact that the
hepatitis B vaccine consists of a series, rather than a single vaccination,
is a key consideration when designing effective strategies for implementing
this requirement. Communication between providers and schools regarding immunization
status will be essential to capitalize on the strengths of both entities.
This study has 2 main limitations. The first concerns issues of potential
sampling bias and the resultant limitations on generalizability. Forty percent
of the surveys distributed were not returned, raising the issue of potential
nonresponse bias. Latino students were underrepresented in our sample, as
were students who had not begun the immunization series. The extent to which
the underrepresentation of these 2 groups affects the findings is unknown.
Potential bias owing to missing data in the regression analysis was also examined.
Respondents with missing data seemed to be a somewhat more vulnerable group
than those with complete data. More studies are needed to investigate strategies
for immunizing this higher-risk group. Another source of potential bias is
that the schools participating in the study were a convenience sample and
not randomly selected. A final potential source of bias is that surveys were
administered only in English. These potential biases raise cautionary flags
regarding the extent to which the findings from this study can be generalized
beyond the study population. Any generalization should only be made with the
caveats outlined above and with the knowledge that these sources of potential
bias may alter the results for other samples.
The second main limitation is that of parent recall as a measure of
vaccination status. The written vaccination record is often held as the gold
standard for vaccination status since researchers have found that parent recall
can inflate vaccination rates. However, we chose to measure parent recall
because we were concerned that relying on written records in this case would
actually underestimate the true vaccination rate. Given that this was a voluntary,
anonymous, self-administered survey, we were concerned that respondents, while
willing to complete a brief survey, would not be willing to extend that effort
to finding their immunization records and copying this information onto the
survey.
This study raises additional research questions. One issue bearing further
scrutiny is that of the potential collateral benefits of immunization. Adolescents
typically receive far fewer well-child or preventive services than do either
children or adults, interacting with the health care system instead largely
through acute care.17, 20 Hepatitis
B vaccination mandates such as California's represent an opportunity to redesign
adolescent health services to be centered around primary prevention rather
than crisis intervention.21 Ideally, administration
of vaccinations should be integrated with other preventive services to adolescents,7, 21 such as those outlined in the Guidelines
for Adolescent Preventive Services.22 Further
research is necessary to assess whether adolescents receiving their immunizations
in health care provider offices actually receive these collateral benefits
and what effect, if any, receiving immunizations at schools has on receipt
of these services.
Another issue needing further scrutiny is the costs to the public and
private sectors of such an initiative, and how those costs are apportioned.
Research is needed to answer questions, such as the following: How will commercial
and publicly funded health plans, schools, and communities share the cost
of such an initiative? To what extent are redundant costs incurred, for example,
children receiving a publicly funded vaccine at school despite being insured?
How can policy makers craft the law to ensure equitable and efficient cost
sharing?
AUTHOR INFORMATION
What This Study Adds
Hepatitis B is one of the most prevalent infectious diseases worldwide,
despite the availability of an effective vaccine. Adolescents are at increased
risk for hepatitis B infection and several states have begun passing laws
requiring proof of immunization prior to middle school enrollment. By examining
the correlates of hepatitis B vaccination status in the year prior to implementation
of California's mandate, this article provides insight into the role the medical
and school communities may play in ensuring coverage. Logistic regression
analysis shows that both medical (recency of a well-child visit and hearing
about the law from a health care provider) and school (having an on-campus
vaccination clinic) factors were important in vaccination status, while insurance
status was not. A multifaceted strategy may be most appropriate for successful
coverage of an adolescent population with a vaccination series such as hepatitis
B.
Accepted for publication March 27, 2001.
This research was supported by a Cooperative Agreement between the Centers
for Disease Control and Prevention, and the Association of Schools of Public
Health, Washington, DC, Project S0534-17.
From the Center for Child Health Outcomes, Children's Hospital and
Health Center (Dr Seid and Mss Simmes and Leah); and the Graduate School of
Public Health, San Diego State University (Dr Peddecord and Mss Linton and
Edwards), San Diego, Calif.
Corresponding author and reprints: Michael Seid, PhD, Center for
Child Health Outcomes, Children's Hospital and Health Center, 3020 Children's
Way, MC505, San Diego, CA 92123 (e-mail: mseid{at}chsd.org).
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