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Hepatitis B Vaccination Practices in Hospital Newborn Nurseries Before and After Changes in Vaccination Recommendations
Sarah J. Clark, MPH;
Michael D. Cabana, MD, MPH;
Tasneem Malik, MPH;
Hussain Yusuf, MBBS, MPH;
Gary L. Freed, MD, MPH
Arch Pediatr Adolesc Med. 2001;155:915-920.
ABSTRACT
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Background Routine use of hepatitis B vaccine for low-risk newborns was suspended
on July 7, 1999, because of concern about the potential risk of thimerosal,
a mercury-containing vaccine preservative. Reinstatement of the birth dose
was recommended when a thimerosal-free vaccine became available.
Objective To explore changes in hepatitis B vaccination practices for newborns
related to the revised recommendations for low-risk infants (in this study,
the terms newborn and infant
are used interchangeably).
Design A telephone survey of a random sample of 1000 US hospitals.
Participants Nurse managers, nursery directors, and staff nurses of the newborn nurseries.
Main Outcome Measures Nursery vaccination practices before and after July 7, 1999, and the
availability and use of thimerosal-free vaccine.
Results Interviews were conducted with 773 (87%) of 886 eligible hospitals.
Before July 7, 1999, 78% of the hospitals reported vaccination practices that
were consistent with recommendations at that time, although only 47% vaccinated
all low-risk infants at birth. After July 7, 1999, almost all hospitals discontinued
vaccination of low-risk infants, in accordance with the recommendation change;
however, there was a 6-fold increase in the number of hospitals that were
not vaccinating all high-risk infants. After the introduction of thimerosal-free
vaccine, only 39% of the hospitals reported vaccinating all low-risk infants.
Conclusions Most hospital nurseries altered their newborn hepatitis B vaccination
practices consistent with changes in national recommendations. However, unintended
consequences included the failure of some hospitals to continue vaccinating
all high-risk infants and the delay in reintroducing vaccination for low-risk
newborns after the introduction of a thimerosal-free vaccine. Assessments
of the appropriateness of this country's response to the threat of thimerosal
in vaccines should consider these findings.
INTRODUCTION
THIMEROSAL, an organic mercury-containing preservative, has been used
for more than 60 years in vaccines to prevent contamination. A 1999 report
from the US Agency for Toxic Substances and Disease Registry suggested that
infants who receive thimerosal-containing vaccines in the first 6 months of
life may be exposed to mercury levels exceeding some federal guidelines, and
on July 7, 1999, the US Public Health Service (PHS) and the American Academy
of Pediatrics (AAP) published a joint statement regarding thimerosal.1 Concern about the potential risk related to thimerosal
led the PHS and AAP to change their hepatitis B vaccination recommendation
for low-risk infants, ie, those born to mothers whose test result for hepatitis
B surface antigen (HBsAg) was negative: physicians were encouraged to postpone
the first dose of hepatitis B vaccine from birth until 2 to 6 months of age.
The statement clarified that, due to the high risk of infection, infants born
to mothers who are HBsAg positive or whose HBsAg status is unknown should
continue to receive the first dose of hepatitis B vaccine at birth. This recommendation
was published in Pediatrics,1 Morbidity and Mortality Weekly Report,2
and the AAP News; presented on the National Immunization
Program Web site; and disseminated via state immunization programs and the
AAP's electronic membership mailing list. In addition, the American Academy
of Family Physicians issued its own similar recommendation3
about thimerosal and hepatitis B vaccine. A follow-up statement4
from the PHS stated that a return to the recommended practice of vaccinating
newborns was anticipated as soon as adequate supplies of thimerosal-free vaccine
became available.
On September 10, 1999, a subsequent statement5
was published in Morbidity and Mortality Weekly Report,
announcing the availability of a thimerosal-free hepatitis B vaccine. The Morbidity and Mortality Weekly Report statement5 indicated that a single-antigen thimerosal-free hepatitis
B vaccine should be prioritized for newborns, and that routine hepatitis B
vaccination policies for all newborns should be reintroduced immediately in
hospitals in which such policies and practices had been discontinued. At that
point, thimerosal-free vaccine could be ordered directly from the manufacturer
but was not yet available through the PHS or state immunization programs;
supplies of this vaccine were insufficient at that time to vaccinate all newborns
in the United States. In mid-October 1999, thimerosal-free vaccine became
available through the PHS; states were able to order limited quantities of
the vaccine, prioritized for hospital nurseries only. By December 1999, there
was sufficient vaccine supply to cover the 0- to 6-month age group in all
states.
To explore changes in hepatitis B vaccination practices in hospital
nurseries related to the recommendation changes, a telephone interview study
was designed and conducted in late 1999. Specifically, we sought to characterize
nursery vaccination practices at 3 points: time 1, from January to June 1999,
before any thimerosal-related announcements; time 2, from July to October
1999, during the period that newborn hepatitis B vaccination was suspended
for infants born to HBsAg-negative mothers; and time 3, from November to December
1999, after thimerosal-free vaccine became available in sufficient supply
for all US newborns.
PARTICIPANTS AND METHODS
A standardized 10-minute telephone interview protocol was designed for
use with nurse managers and/or other knowledgeable staff of hospital newborn
nurseries. Specific questions focused on the 3 periods of interest. To estimate
hepatitis B vaccination practices in each period studied, interviewers asked
hospital respondents to indicate whether none, some, or all infants born to
mothers who were HBsAg positive, HBsAg negative, or HBsAg unknown received
hepatitis B vaccine in the newborn nursery before hospital discharge. Other
items focused on the availability of thimerosal-free vaccine; whether resumption
of hepatitis B vaccination was met by any resistance from physicians, nursing
staff, or parents; and demographic variables.
Interview protocols were pilot tested for clarity and ease of use with
nurse managers from a convenience sample of 10 hospitals in 4 states. For
5 of those hospitals, identical interview protocols were used with physician
directors of the newborn nursery. Information provided by nurse managers was
validated by physician nursery directors using identical interview protocols.
Data collection occurred in December 1999, 2 to 3 months after
publication of the PHS recommendation to resume newborn vaccination; by this
time, there was a sufficient supply of thimerosal-free vaccine available to
vaccinate all US newborns. Six trained interviewers telephoned a national
random sample of 1000 hospitals, drawn from the database of all hospitals
maintained by the Hospital Management Research Institute. Interviewers asked
to speak with the nurse manager in charge of the normal newborn nursery. If
a nurse manager was unavailable, interviewers asked to speak with the nursery
director or a charge nurse. If that respondent felt unable to provide reliable
information (eg, had worked in the nursery <6 months or had administrative
oversight rather than day-to-day involvement), she or he recommended a staff
nurse knowledgeable about nursery vaccination practices to complete the interview.
When the appropriate individual was located, interviewers obtained verbal
consent to participate and then conducted the interview.
Data analysis included general descriptive statistics, followed by bivariate
analysis to explore associations between hospital demographic characteristics
and hepatitis B vaccination practices. Analyses were performed using SAS statistical
software, version 6.0 (SAS Institute Inc, Cary, NC). The study protocol was
approved by the institutional review boards of the University of Michigan
Medical Center, Ann Arbor, and the Centers for Disease Control and Prevention,
Atlanta, Ga.
RESULTS
RESPONSE RATE
From our original sample of 1000 hospitals, we excluded 114 ineligible
hospitals (those that had closed or that were not delivering newborns). Interviews
were conducted with 773 of 886 eligible hospitals, for a response rate of
87%. Of the nonparticipating hospitals, 86 (10%) cited inadequate time to
complete the interview and 27 (3%) declined participation.
DEMOGRAPHIC CHARACTERISTICS
Most interviews were completed with the normal newborn nursery's nurse
manager (64%); other interviewees included charge nurses (12%), staff nurses
(16%), or physician nursery directors (8%). The demographic characteristics
of hospitals with completed interviews are shown in Table 1. These hospitals represented all 50 states, plus the District
of Columbia.
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Table 1. Demographic Characteristics of the 773 Responding Hospitals
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VACCINATION PRACTICES
As shown in Table 2, 88%
of the hospitals in the study gave hepatitis B vaccine to all infants born
to HBsAg-positive mothers, with an additional 9% reporting no mothers who
were HBsAg positive during time 1. Vaccination of other infant groups at time
1 was less consistent, with only 47% of hospitals vaccinating all low-risk
infants (those born to mothers who were HBsAg negative). At time 2, most hospitals
altered their vaccination practices in accordance with the PHS/AAP revised
recommendations; however, a small but significant number of hospitals reported
vaccination practices for high-risk infants that were inconsistent with the
time 2 recommendations. Specifically, 7% of hospitals reported vaccinating
none of the infants born to HBsAg-positive mothers, and 19% of hospitals reported
vaccinating none of the infants born to mothers of unknown HBsAg status; these
time 2 figures represent a 6-fold increase over the time 1 rates. In addition,
many more hospitals reported that they had no mothers whose HBsAg status was
positive or unknown during time 2 compared with time 1.
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Table 2. Hepatitis B Vaccination Practices, Based on Hospital Respondent
Estimates*
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INTRODUCTION OF THIMEROSAL-FREE VACCINE
At the time of the interview, only 223 hospitals had obtained thimerosal-free
vaccine for their nursery. Among the 405 hospitals that did not have thimerosal-free
vaccine, 61% either were unaware that the product was available or had not
made a decision about its use; for another 7%, the hospital had decided not
to reinstitute hepatitis B vaccination. Twenty-seven percent of hospitals
had ordered vaccine and were awaiting delivery from either the vaccine manufacturer
or the state vaccine program.
For the 223 hospitals using thimerosal-free vaccine available at the
time of the interview, respondents were asked whether there was resistance
from physicians, parents, or nursing staff to the resumption of hepatitis
B vaccination in the nursery. Sixteen percent believed there was some or a
lot of resistance from physicians, 9% believed there was resistance from parents,
and 7% believed there was resistance from nursing staff. Nineteen percent
reported that confusion about the changes in hepatitis B vaccine recommendations
may have affected their nursery's vaccination practices. In addition, 27%
of hospital respondents indicated there were one or more "other" factors affecting
the use of hepatitis B vaccine in the newborn nursery. The factors described
most frequently were physician preference to administer all doses of hepatitis
B vaccine in the outpatient setting (n = 29), the high cost of thimerosal-free
vaccine and/or reimbursement problems in the hospital setting (n = 20), and
concerns about insufficient supply of thimerosal-free vaccine (n = 10).
Hepatitis B vaccination practices at time 3 for the 223 hospitals with
thimerosal-free vaccine are shown separately for each risk group in Table 2. These data demonstrate that, for
infants born to HBsAg-positive mothers, 95% of hospitals either vaccinated
all such infants or had no infants in this group; this is comparable to the
time 1 rates. However, the proportion of hospitals vaccinating all low-risk
infants was smaller at time 3 than at time 1.
Bivariate analyses were conducted to explore associations between vaccination
practices for low-risk infants at times 1 and 3. Among hospitals that were
vaccinating all low-risk infants at time 1 and that had thimerosal-free vaccine
available at time 3, those that reported physician resistance to resumption
of newborn vaccination were less likely to be vaccinating all low-risk infants
at time 3 (38% vs 62%; P = .02), as were those that
reported some confusion related to the policy change (45% vs 55%; P = .02).
CONSISTENCY OF VACCINATION PRACTICES WITH PHS/AAP RECOMMENDATIONS
Table 3 classifies hospitals'
hepatitis B vaccination practices at all 3 periods. At time 1, most hospitals
had vaccination practices that were consistent with PHS/AAP recommendations
at that time (ie, vaccinating all infants born to mothers with positive or
unknown hepatitis B status). The recommendation did not require that infants
receive a birth dose of hepatitis B vaccine, only that the first dose be received
at or by the age of 2 months; therefore, hospitals that were not vaccinating
all low-risk infants were not categorized as inconsistent with recommendations.
At time 2, only 55% of the reported vaccination practices were consistent
with PHS/AAP recommendations (ie, vaccinating all infants born to mothers
with positive or unknown hepatitis B status but none of the low-risk infants).
The primary reason for this decrease was failure to vaccinate all infants
born to mothers of unknown hepatitis B status (34% of hospitals); in addition,
6% of hospitals were categorized as inconsistent because they continued vaccinating
all low-risk newborns. At time 3, only 37% of hospitals with thimerosal-free
vaccine available reported vaccination practices consistent with PHS/AAP recommendations
for universal vaccination of all newborns. Of the 63% of hospitals that were
inconsistent at time 3, each reported vaccinating none or some—but not
all—infants of unknown status; not one hospital in this group had resumed
universal vaccination of low-risk newborns.
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Table 3. Consistency of Hospital Vaccination Practices With PHS/AAP
Recommendations*
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COMMENT
Data from this study suggest that changes in hospital hepatitis B vaccination
practices in response to revised PHS/AAP recommendations had some unintended
and potentially harmful effects. Although more than 90% of hospitals suspended
the use of thimerosal-containing vaccine for infants born to HBsAg-negative
mothers, some hospitals discontinued routine vaccination practices for high-risk
infants and for infants at unknown risk. The proportion of hospitals vaccinating
none of the infants born to HBsAg-positive mothers increased from 1% at time
1 to 7% at time 2; the proportion of hospitals vaccinating none of the infants
born to mothers whose HBsAg status was unknown also increased during this
period, from 3% to 19%. This finding is extremely concerning, considering
the significant medical implications resulting from failure to administer
hepatitis B vaccine to high-risk infants in the first 12 hours of life. During
data collection for this study, interviewers verified responses of inappropriate
vaccination practices for high-risk infants through follow-up questions (eg,
"So none of the infants born to HBsAg-positive mothers were vaccinated?").
This study's reported increase in inappropriate vaccination practices for
a small group of high-risk infants parallels anecdotal reports to the PHS
that, following publication of the thimerosal-related recommendations, some
high-risk infants did not receive hepatitis B vaccine within 12 hours of birth.5
Our data do not clarify whether reported nonvaccination of all high-risk
infants was due to misinterpretation of new recommendations, breakdowns in
communication from nursery director to nurse managers or other nursing staff,
or human error. Although one fifth of the respondents thought that confusion
about the changing hepatitis B vaccine recommendations affected their nursery's
vaccination rate, the question was not specific to high-risk patients; however,
other reports6 also have indicated that physicians
were confused by the recommendation changes. In our study, many hospital respondents
made unsolicited or follow-up comments that not all attending physicians were
well-informed about thimerosal issues and the revised recommendations. This
was most problematic in hospitals in which different attending physicians
maintained different standing orders or vaccination preferences; the result
was a situation in which some, but not all, infants were vaccinated. Lack
of information or understanding of the recommendation must be suspected as
a possible factor in the reported failure to vaccinate all high-risk infants,
an unfortunate and unintended consequence of the publicity and recommendation
changes related to thimerosal.
These results serve as a cautionary tale: the policy changes prompted
by the theoretical risk of thimerosal appear to be associated with an increase
in inappropriate vaccination practices for infants who had a real risk of
hepatitis B infection. While this study's methods do not allow for the determination
of a causal link between lack of information or understanding about the recommendation
change and reported failure to vaccinate all high-risk infants, the 6-fold
reported increase in inappropriate vaccination practices for high-risk infants
cannot be discounted. Although such an increase in inappropriate vaccination
practices for high-risk infants was unintended, it could have been predicted.
Previous studies7, 8 have shown
that outpatient primary care physicians can be confused about changes in childhood
immunization recommendations. A somewhat greater level of confusion would
be expected for newborn hepatitis B vaccine, as a broader array of parties—physician
nursery directors, nurse managers, hospital pharmacists, and outpatient primary
care physicians—are involved in vaccination decisions, and then those
decisions must be conveyed consistently and accurately to staff responsible
for vaccinating individual patients.
Also concerning is the decreased rate of hepatitis B vaccination for
low-risk newborns in the study's time 3 period, among hospitals that had thimerosal-free
vaccine. The proportion of hospitals vaccinating all low-risk infants decreased
from 47% at time 1 to 39% at time 3. Certainly, this study was conducted at
a time when vaccination practices at many hospitals were in flux, and we would
expect that some hospitals that had not yet resumed universal newborn vaccination
did so as thimerosal-free vaccine became more widely available. However, it
is also possible that this lower vaccination rate may signal a long-term shift
toward administration of the initial dose of hepatitis B vaccine in the outpatient
setting. Comments from the respondents in this study indicate that many primary
care physicians prefer to begin the hepatitis B vaccine series in the outpatient
office setting, because of the convenience of record keeping, the ability
to use combined hepatitis B and Haemophilus influenzae
type b vaccine, and increased reimbursement. Although these preferences likely
existed before the thimerosal-related policy changes, the July 7, 1999, recommendation
to shift the first hepatitis B vaccine dose to the outpatient setting provided
the impetus to implement the change and "opened the door" to allowing physicians
to realize the benefits of giving all doses in the outpatient setting. Afterward,
resumption of newborn vaccination required not only the availability of thimerosal-free
vaccine but also the convincing of outpatient primary care physicians that
the benefits of newborn vaccination outweighed the convenience of beginning
the series at the age of 2 months.
Furthermore, the introduction of thimerosal-free vaccine did not happen
in a timely fashion. In this study, at time 3—when the nation's vaccine
supply was sufficient for all infants aged 0 to 6 months—61% of hospitals
that were not using thimerosal-free vaccine either did not know the vaccine
was available or had not gotten around to making a decision regarding its
use. This lack of information and/or action extended the period during which
low-risk newborns were not vaccinated.
The suspension of routine vaccination for low-risk infants, and the
delay in its resumption, appears even more problematic in the face of inaccurate
or inconsistent communication of information between prenatal providers and
birthing facilities. Such was the case of a December 1999 death of a 3-month-old
Michigan infant, born to an HBsAg-positive woman whose HBsAg status was communicated
incorrectly to the birthing hospital.9 The
hospital had not resumed routine vaccination of low-risk newborns, even though
thimerosal-free vaccine was available. The infant received neither hepatitis
B immunoglobulin nor hepatitis B vaccine during the hospital stay, and died
less than 2 weeks after the onset of acute hepatitis B infection. While the
cause of death was directly linked to the error in information transfer about
the mother's hepatitis B status, the suspension of universal newborn vaccination
for low-risk infants served to remove what would have been a "safety net"
protection for this infant.
This situation illustrates a tension between establishing a protection
against a theoretical risk and the possible unintended consequences of that
action that carry an actual risk. When setting a policy, and when evaluating
its impact, the counterplay between theoretical and actual risk, and the potential
tradeoffs that any policy change can inspire, must be studied. In this case,
the policy change driven by a theoretical risk from thimerosal produced an
indirect and unintended—but still clinically significant—risk
of hepatitis B infection in a small but significant number of infants. Knowing
that policy changes cause disruptions that lead to problems of implementation,
the known and potential impacts of policy changes, positive and negative,
should be factored into policy decisions. This perspective is already used
in other policy arenas, such as environmental impact statements that are called
for before making important environmental policy changes. Future immunization
policy changes should strive to incorporate assessment of possible unintended
consequences into the policy's benefit equation.
This study has several limitations that may affect its ability to draw
definitive conclusions. First, responses consisted solely of respondent self-report.
Verification of hospital policies, vaccination rates, and demographic characteristics
was not performed. However, we believe that the hospital respondents in this
study were well-informed about nursery vaccination practices, and our results
are consistent with another report9 from the
Centers for Disease Control and Prevention regarding changes in hepatitis
B vaccination policies and standing orders after the PHS/AAP recommendation
changes. More important, individual reports of inappropriate vaccination practices,
such as the failure to administer hepatitis B vaccine to an infant of an HBsAg-positive
mother, were not examined, thus prohibiting us from demonstrating any causal
link between reported inappropriate vaccination practices and other factors,
including lack of information or understanding of hepatitis B vaccination
recommendations. Finally, we did not attempt to characterize nonrespondent
hospitals; however, the study's high response rate (87%) and low number of
refusals (n = 27) allow us to conclude that the sample is representative of
all US hospitals.
CONCLUSIONS
Most hospital nurseries altered their newborn hepatitis B vaccination
policies and practices in ways that were consistent with changes in national
recommendations from the PHS and national physician groups. However, unintended
consequences of these recommendation changes include the reported failure
of some hospitals to continue to vaccinate all high-risk infants after the
policy change, even though all PHS and AAP statements clearly indicated that
vaccination should continue for such infants. A further consequence is the
reluctance of some hospitals to resume universal vaccination of low-risk newborns
after thimerosal-free vaccine became available. Such unintended consequences
must be included in any assessment of the appropriateness and relative success
of this country's response to the threat of thimerosal in vaccines.
AUTHOR INFORMATION
What This Study Adds
The suspension of newborn hepatitis B vaccination for low-risk infants
was a controversial policy, related to a theoretical risk of mercury exposure.
The Centers for Disease Control and Prevention and physician specialty societies
had no direct means to identify and inform hospital decision makers for nursery
vaccination issues, to ensure appropriate and consistent response to the policy
change. This study describes the implementation of the recommendation to suspend,
and then resume, newborn hepatitis B vaccination. The variability of hospital
responses and the delayed resumption of newborn vaccination point to the need
for better methods of communication about policy changes and a more thoughtful
balance between theoretical risk and actual risks related to inconsistent
implementation.
Accepted for publication April 1, 2001.
This study was funded by the Centers for Disease Control and Prevention,
Atlanta, through a cooperative agreement with the Association of Teachers
of Preventive Medicine, Washington, DC.
The 2 authors affiliated with the Centers for Disease Control and Prevention,
Ms Malik and Dr Yusuf, participated as individuals in the design of the study,
the interpretation of results, and the review/revision of the manuscript.
From the Child Health Evaluation and Research Unit, Division of General
Pediatrics, University of Michigan, Ann Arbor (Ms Clark and Drs Cabana and
Freed); and the National Immunization Program, Centers for Disease Control
and Prevention, Atlanta, Ga (Ms Malik and Dr Yusuf).
Corresponding author and reprints: Sarah J. Clark, MPH, Division
of General Pediatrics, University of Michigan, 300 N Ingalls Bldg, Room NI6E06,
Ann Arbor, MI 48109-0456 (e-mail: saclark{at}med.umich.edu).
REFERENCES
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1. Joint statement of the American Academy of Pediatrics (AAP) and the
United States Public Health Service (USPHS). Pediatrics. 1999;104(pt 1):568-569.
2. Thimerosal in vaccines: a joint statement of the American Academy of
Pediatrics and the Public Health Service. MMWR Morb Mortal Wkly Rep. 1999;48:563-565.
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3. American Academy of Family Physicians. Policy statement of the American Academy of Family Physicians on thimerosal
in vaccines, July 8, 1999. Available at: http://www.aafp.org/policy/camp/20.html.
Accessed June 1, 2000.
4. Centers for Disease Control and Prevention. Implementation guidance for immunization grantees during the transition
period to vaccines without thimerosal. Available at: http://www.cdc.gov/nip/news/thimerosal-guidance.html. Accessed July 14, 1999.
5. Availability of hepatitis B vaccine that does not contain thimerosal
as a preservative. MMWR Morb Mortal Wkly Rep. 1999;48:780-782.
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6. Halsey NA. Limiting infant exposure to thimerosal in vaccines and other sources
of mercury. JAMA. 1999;282:1763-1766.
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7. Freed GL, Freeman VA, Clark SJ, Konrad TR, Pathman DE. Pediatrician and family physician agreement with and adoption of universal
hepatitis B immunization. J Fam Pract. 1996;42:587-592.
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PUBMED
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