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Delays in Receipt of Immunizations in Low-Birth-Weight Children
A Nationally Representative Sample
Diane L. Langkamp, MD, MPH;
Stacy Hoshaw-Woodard, PhD;
Mark E. Boye, MS, MBA, MPH;
Stanley Lemeshow, PhD
Arch Pediatr Adolesc Med. 2001;155:167-172.
ABSTRACT
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Background Studies of very low-birth-weight (VLBW) children discharged from neonatal
intensive care units have shown delays in receipt of routine childhood immunizations.
However, a recent study of VLBW children in 3 health maintenance organizations
found no significant delays in immunizations.
Objective To assess the risk of immunization delays for moderately low-birth-weight
(MLBW; 1500 g-2499 g) and VLBW (<1500 g) children compared with normal-birth-weight
children in a nationally representative birth sample.
Design Logistic regression analysis using the 1988 National Maternal and Infant
Health Survey and the 1991 Longitudinal Follow-up Survey.
Setting Nationally representative sample of children born in 1988 in the United
States.
Participants A total of 8285 children whose mothers completed both surveys.
Main Outcome Measures Age at receipt of each of the first 4 doses of diphtheria and tetanus
toxoids and pertussis vaccine, the first 3 doses of polio vaccine, and the
first dose of measles-mumps-rubella vaccine for MLBW and VLBW children, and
normal-birth-weight children. We also examined whether children were up-to-date
for all immunizations at ages 12, 24, and 36 months based on birth-weight
groups.
Results Very low-birth-weight children received their first 3 doses of diphtheria
and tetanus toxoids and pertussis vaccine and their first 2 doses of polio
vaccine significantly later than normal-birth-weight children (P <.001). Very low-birth-weight children were significantly less
likely to be up to date for all immunizations at ages 12 months (odds ratio
[OR] = .556; P = .001), 24 months (OR = .439; P <.001), and 36 months (OR = .446; P <.001) compared with normal-birth-weight children.
Conclusion Very low-birth-weight children are at risk for immunization delays compared
with normal-birth-weight children.
INTRODUCTION
DESPITE remarkable advances in vaccine development and programs to increase
access to immunizations, many children younger than 3 years do not receive
their routine immunizations on time. Although interventions to improve immunization
rates have been studied, most programs designed to increase immunization rates
among young children have focused on the poor or uninsured.1, 2, 3, 4
Prematurely born children are at an increased risk to contract vaccine-preventable
diseases such as pertussis.5 Premature children
with pertussis are at greater risk for severe disease and hospitalization.5 Although the American Academy of Pediatrics Committee
on Infectious Diseases has recommended that premature children receive immunizations
at the same chronological age as full-term children,6
primary care physicians remain hesitant to immunize preterm children who have
complex medical histories.7 Some primary care
physicians and parents of preterm children mistakenly believe that other factors
such as birth weight, current weight, or degree of prematurity should influence
the timing of immunizations for preterm children.7, 8
Thus, even though preterm children can mount adequate immune responses when
immunized at the recommended chronological age,9
they often receive immunizations on a delayed schedule.10
Most previous research on immunization in preterm, low-birth-weight
(LBW) children has been limited to children who have been hospitalized in
a single neonatal intensive care unit (NICU). Vohr and Oh10
demonstrated that LBW children previously hospitalized in their NICU received
the first 3 doses of diphtheria and tetanus toxoids and pertussis (DTP) on
a delayed schedule. Magoon et al11 demonstrated
delays in both DTP and polio immunizations in LBW children who had been hospitalized
in their NICU. However, the findings of these investigations may not be generalizable.
Because some LBW infants do not require admission to an NICU, their experiences
are not captured by such center-based studies. Similarly, studies that assess
immunization rates of LBW children in a health maintenance organization12 fail to evaluate the effect of insurance status on
immunization delays.
To better understand the effect of LBW on immunization practices, we
examined data from the 1988 National Maternal and Infant Health Survey (NMIHS)
and the 1991 Longitudinal Follow-up Survey to explore the relationship between
LBW and immunization delays in a nationally representative sample. Although
these surveys are several years old, they remain the only nationally representative
data sets that provide detailed individual-level data on the health experiences
of children during their first 3 years of life. Although there have been many
efforts to improve immunization rates in young children during the last few
years, none of these have been specifically directed at LBW children. Thus,
the absolute rate of on-time immunizations may have increased among children
younger than 3 years, but there is no reason to believe that the relative
differences in immunization delay between LBW and normal-birth-weight (NBW)
children has changed since the NMIHS and 1991 Longitudinal Follow-up Survey
data were collected. The purpose of this study was to determine, in a nationally
representative sample, whether moderately low-birth-weight (MLBW) and very
low-birth-weight (VLBW) children are at increased risk of immunization delays
up to 36 months of age compared with NBW children. The study focuses on the
child's age at receipt of the first 4 doses of DTP, the first 3 doses of polio
vaccine, and the first dose of the measles-mumps-rubella vaccine (MMR) (4:3:1
series).
METHODS
DATA SOURCE
This investigation analyzed data from the 1988 NMIHS and the 1991 Longitudinal
Follow-up Survey.13, 14 The 1988
NMIHS used a nationally representative sample of 9953 children born in the
United States that year and linked birth certificate data to surveys of mothers.
African American and LBW children were oversampled. The mothers of 8285 children
participated in both the 1988 and 1991 surveys; these 8285 mothers and their
children are the subjects of this study. The child's age at receipt of each
vaccine was based on provider records.
The 1991 Longitudinal Follow-up Survey asked the participating mothers
to list all outpatient or inpatient settings where the index child had received
medical care since birth. Each provider listed was subsequently contacted
and asked to answer several questions, including an inquiry about immunizations
administered at each visit; alternatively, providers could choose to send
a copy of the child's medical record from each visit or hospitalization. No
provider information was available for 2209 children (27%) because either
the mother did not list any providers, or none of the listed providers returned
the survey. Because not all the providers listed by the mother returned the
survey, 2226 children (27%) had incomplete provider information. Of those
with incomplete provider information, 380 children had documentation of receipt
of all 8 immunizations examined in this study. These children were reclassified
as "complete" with respect to immunization records. The provider records included
only the type of immunization and the month and year of administration, but
did not indicate which dose in the series the immunization represented. For
the children with some immunizations but incomplete provider records, there
is no way of knowing which doses were missing. Thus, 2209 children had no
immunization data, 1846 had incomplete immunization data, and 4230 had complete
immunization data.
Because the goal of this study was to use population estimates to examine
the timing of immunizations for VLBW, MLBW, and NBW children, and because
there were many cases with missing and incomplete immunization records, we
redistributed the statistical weights of those children with missing or incomplete
immunization data to children of similar demographic characteristics who had
complete provider records. To do this, 864 subgroups were created using the
demographic variables of insurance for prenatal health care, place of residence
(urban, rural), household income in 1988 (<$20 000 or  $20 000),
maternal age at child's birth (17-20 years, 21-34 years, 35 years), maternal
level of education (< high school graduate, high school graduate, some
college or other formal education beyond high school), mother's marital status,
mother's race, and the child's birth weight (<1500 g, 1500-2499 g, 2500
g). These characteristics were chosen because the complete and incomplete
cases showed significant differences in these variables. The statistical weights
of those cases in the missing/incomplete groups that fell into a subgroup
defined by these demographic variables were added up and redistributed equally
among those cases in the subgroup with complete provider records. For some
subgroups, there were cases in the missing/incomplete group but no corresponding
cases in the complete group. In these situations, the cases were assigned
to a similar subgroup based on a 1-level change in one of the variables. These
cases were matched on 7 of the 8 variables. Most often, the change in level
was in maternal age, household income, or maternal education. Because these
were continuous variables that had been categorized, the case was reassigned
to the subgroup with the closest characteristics to the one that could not
be matched. For example, if the mother's age was 22 years, the case was matched
on 7 of 8 variables and reassigned to the 17 to 20 years subgroup, not the
35 years or older subgroup. The 4230 children with complete provider records
were reweighted to represent the 3 898 922 children born alive in
the United States in 1988. This redistribution of weights is a form of imputation
such that the cases with the incomplete data are represented by all of the
complete cases with similar demographic characteristics.
For purposes of this study, VLBW was defined as less than 1500 g. Moderately
low birth weight was defined as 1500 g to 2499 g. Low birth weight was defined
as less than 2500 g. Normal birth weight was defined as 2500 g or greater.
In the sample, 447 children (10.6%) were classified as VLBW and represented
1.2% of the population of live births, and 648 children (15.3%) were classified
as MLBW and represented 5.7% of the population of live births. Only immunizations
administered during visits when the child was aged 36 months or younger were
included in this study.
ANALYSIS
The mean age at receipt of each dose of DTP, each dose of polio vaccine,
and MMR was compared for VLBW, MLBW, and NBW children using an adjusted Wald
statistic.15 Contingency tables were created
for the age at immunization by birth weight groups and the relationship was
tested with an F statistic that accounts for the survey design.
The relationship between birth-weight groups and whether the infant
was up-to-date (UTD) for all recommended immunizations at 12 months, 24 months,
and 36 months of age was assessed using logistic regression models. The goal
of this analysis was to assess the relationship between birth weight and immunization
status, not to develop a predictive model of immunization status. Therefore,
other variables were added to the logistic regression model only when they
were determined to be confounders or effect modifiers, not when they were
significant predictors of immunization status. Confounders were defined as
variables that, when controlled for, significantly alter the odds ratio (OR)
for birth-weight group.16 In this analysis,
to be considered a confounder, the variable had to (1) elicit a 15% change
in the OR for birth-weight group and (2) have no more than 5% of the values
missing. Effect modifiers were defined as variables that have a significant
interaction with birth-weight group.16 This
is manifested by the ORs for birth weight groups being different for different
levels of the effect modifier. To be considered an effect modifier (1) the
interaction between the variable and birth-weight group had to be significant
at the P = .01 level, (2) the variable had to have
no more than 5% of the values missing, and (3) the joint occurrence of birth
weight group and the effect modifier had to occur in at least 5% of the subjects.
All analyses were performed using STATA survey commands17
to account for the complex survey design.
RESULTS
Table 1 and Table 2 present the mean age at which VLBW, MLBW, and NBW children
received their first and second doses of DTP and polio vaccines. Very low-birth-weight
and MLBW children received their first and second doses of DTP, and their
first and second doses of the polio vaccine significantly later than NBW children.
Very low-birth-weight children also received their third DTP vaccine significantly
later than NBW children, but this was not true for MLBW children. There was
no significant difference between VLBW and NBW children or MLBW and NBW children
for age at receipt of the fourth dose of DTP, third dose of polio, or MMR
among children who received these immunizations in the first 36 months of
life.
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Table 1. Comparison Between Birth-Weight Groups for Mean Age at First
Diphtheria and Tetanus Toxoids and Pertussis and Polio Immunizations*
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Table 2. Comparison Between Birth Weight Groups for Mean Age at Second
Diphtheria and Tetanus Toxoids and Pertussis and Polio Immunizations*
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Table 3 provides the crude
OR for the effect of birth weight on children being UTD for all immunizations
at 12 months, 24 months, and 36 months of age. Very low-birth-weight and MLBW
children were significantly less likely to be UTD for all immunizations at
12 months of age (3 doses of DTP and 2 doses of polio) and at 24 months and
36 months of age (4:3:1) than were NBW children. No demographic or neonatal
variables met the criteria to be considered as confounding variables for UTD
at 12 months, 24 months, or 36 months of age.
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Table 3. Crude Odds Ratios From Logistic Regressions of Birth Weight
and Immunization Status at Ages 12, 24, and 36 Months*
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Table 4 presents the ORs
of being UTD at 12 months of age for VLBW children compared with NBW children,
stratified on the mother's level of education and whether the child was covered
by private health insurance. Table 5
provides the corresponding percentages of each birth-weight group, stratified
on the same 2 variables. These variables, private health insurance coverage
for the child and maternal level of education, showed a significant interaction
between VLBW and UTD at 12 months of age, and thus were the only variables
considered to be effect modifiers at this age. Among children not covered
by private health insurance, VLBW children were significantly less likely
to be UTD at 12 months of age than were NBW children (OR = .215; P<.001). Among children covered by private health insurance, the
odds of being UTD at 12 months of age for VLBW children were no different
than the odds for NBW children (OR = .880; P = .54).
Among children whose mothers had less than a high school education, VLBW children
were significantly less likely to be UTD at 12 months of age than were NBW
children (OR = .103; P = .002). Among children whose
mothers had completed high school, the odds of being UTD at 12 months of age
for VLBW children were no different than the odds of being UTD for NBW children
(OR = .575; P = .07).
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Table 4. Stratified Odds Ratios by Effect Modifiers for Up-to-Date
Immunization Status at Age 12 Months*
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Table 5. Stratified Percentages by Effect Modifiers for Up-to-Date
Immunization Status at Age 12 Months*
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Table 6 and Table 7 present the ORs for being UTD at 24 months of age for VLBW
and MLBW children compared with NBW children and the corresponding percentages
of each birth-weight group stratified on whether or not the mother's prenatal
care was covered by insurance. Only this variable, whether or not the mother's
prenatal care was covered by health insurance, showed a significant interaction
with LBW and UTD at 24 months of age, and was thus considered an effect modifier.
Low-birth-weight children whose mother's prenatal care was not paid for by
insurance were significantly less likely to be UTD at 24 months of age compared
with NBW children (OR = .568; P = .001). In contrast,
if a mother's prenatal care was covered by insurance, the odds of LBW children
being UTD at age 24 months was no different than that of NBW children (OR
= .927; P = .56). No variables met the criteria to
be considered an effect modifier at 36 months of age.
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Table 6. Stratified Odds Ratios by Effect Modifiers for Up-to-Date
Immunization Status at Age 24 Months*
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Table 7. Stratified Percentages by Effect Modifiers for Up-to-Date
Immunization Status at Age 24 Months*
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COMMENT
This study is unique for 2 reasons. First, we analyzed a nationally
representative survey with reweighting of the statistical weights to represent
the total number of children born in 1988. Many studies that used these data
sets either discarded the weights of those with missing values18
or conducted the analysis with no weighting.19
Second, the analysis focused on birth weight as the only risk factor for immunization
delay. Additional variables were added to the model only if they were determined
to be confounders or effect modifiers, not because they were significant in
predicting immunization status. The goal of this analysis was not to create
a model to predict immunization status, but to assess the relationship between
birth weight and immunization status.
In this population-based study, VLBW and MLBW children were at significantly
greater risk of immunization delays during the first year of life than NBW
children. Very low-birth-weight and MLBW children remained significantly less
likely to have completed the 4:3:1 series by 36 months of age. The relationship
between LBW and immunization delay was strong, and it remained significant
even after statistically adjusting for many socioeconomic and demographic
variables that have been identified as confounding variables in other immunization
studies.
Our findings stand in contrast to those of Davis et al,12
who reported that children "born prematurely were vaccinated at levels approaching
that of the general population." Although Davis et al describe their study
as being population-based, their sample was limited to children who were continuously
enrolled in 1 of 3 health maintenance organizations from birth to 24 months
of age. Other studies have shown that a lack of health insurance or gaps in
health insurance are associated with children having fewer immunizations,
less preventive care, and a lower chance of having a regular source of primary
care.14, 20, 21 Kogan
et al14 demonstrated that nearly one quarter
of children in the United States were without health insurance for at least
1 month during their first 3 years of life. Our study shows that lack of health
insurance significantly increases the risk of immunization delay in VLBW children.
At 12 months of age, VLBW children who lacked private health insurance coverage
were significantly less likely to be UTD than NBW children; whereas VLBW children
with private health insurance were as likely to be UTD as NBW children. The
inclusion of children with diverse backgrounds who received care in a variety
of settings with a variety of financial arrangements to provide their care
may explain much of the difference between our findings and those of Davis
et al.12 Our study emphasizes the critical
role that access to care plays in immunization status of LBW children.
Another factor that may have contributed to the differences between
our findings and those of Davis et al12 is
that the children within a health maintenance organization have a unified
medical record both for primary and subspecialty care. For children who receive
care at multiple sites from multiple providers, lack of access to immunization
records often interferes with timely administration of immunizations.22, 23
Some LBW children may be considered to have special health care needs.
Many LBW children receive subspecialty care in the first year of life for
such problems as chronic lung disease, apnea of prematurity, and retinopathy
of prematurity. Two studies have documented that children with special health
care needs or children seeking subspecialty care are likely to experience
immunization delays.24, 25 Our
study further emphasizes that the focus of improving immunization rates needs
to be broadened to include children with special health care needs.
Our study has several limitations. The most obvious shortcoming is the
age of the data. Immunization recommendations have changed to include more
vaccines (Haemophilus influenzae type B, hepatitis
B, Pneumococcus, varicella) which may make the challenges
of immunizing these small infants even greater. Since the measles outbreak
of 1989-1991, there have been major public health efforts to increase immunization
rates among young children in the United States.26
Despite these changes, there has been no focused effort to address the issue
of immunization delays in LBW children. We suggest 2 possible courses that
immunization practices for LBW children may have taken in the past decade.
First, LBW children, including those with Medicaid or no insurance, now may
be immunized at "rates approaching the general population," as Davis et al12 described. However, a second possibility is that
the absolute immunization rates among LBW children have risen parallel to,
but still lower than, the increase in immunization rates among young children
in general in the United States. If the second scenario is correct, despite
some improvement, LBW children continue to lag behind NBW children in absolute
immunization rates.
A second limitation of our study is that we relied on provider data
for immunization information. In such a large, complex survey, there may have
been incomplete identification of all providers and incomplete reporting from
all providers. Thus, the absolute immunization rates we report may be lower
than the actual rates. However, we believe that the risk of underreporting
would not be any greater among VLBW and MLBW children than among NBW children.
Consequently, the relative relationship between birth weight and immunization
status should not be affected by underreporting. Reliance on provider information
for immunization status is also a strength of our study because other studies
have demonstrated that parents' reports of children's immunization status
are not accurate.27
To our knowledge to date, our study is the first assessment of the relationship
between LBW and immunization delays that used a nationally representative
sample. Because the NMIHS oversampled LBW births, it provides a more robust
estimate of the effect of LBW on immunization status than would be possible
in smaller samples. We found a very strong relationship between LBW and immunization
delays. No variables played an important role as confounding variables, and
only a few variables were significant effect modifiers.
Our study demonstrates a need for intense focus on the relationship
between LBW and immunization status. Further study is needed to gather more
current data about immunization patterns among LBW children and to develop
effective interventions to improve immunization rates in this population.
AUTHOR INFORMATION
Accepted for publication October 13, 2000.
The research was supported by a grant from Children's Research Institute,
Columbus, Ohio.
Presented at the annual meeting of the Pediatric Academic Societies,
Boston, Mass, May 14, 2000.
From the Department of Pediatrics (Dr Langkamp), the Biostatistics
Program (Drs Hoshaw-Woodard and Lemeshow), and the College of Pharmacy (Mr
Boye), Ohio State University, Columbus.
Corresponding author: Diane L. Langkamp, MD, MPH, Children's Hospital,
Room H310, 700 Children's Dr, Columbus, OH 43205 (e-mail: dlangkam{at}chi.osu.edu).
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