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January
2008: VOLUME
1, NUMBER 7
Update on Adult Immunizations
In this Issue...
Immunization
has been a cornerstone of pediatric preventive care
for decades, with routine immunization of children leading
to dramatic reductions in disease incidence, morbidity,
and mortality. Over the past few years, there have been
a growing number of new vaccines licensed and recommended
for adults, including vaccines against human papillomavirus
(HPV), pertussis, and herpes zoster. While vaccination
is an ingrained concept among pediatricians, the notion
of a routine immunization schedule and program for adults
has not taken root, as reflected by the continued low
rates of vaccination for key vaccines among the adult
population.
In this issue, we review recent investigations of vaccines
in the adult population, and discuss new recommendations
on the immunization of adults from the Centers for Disease
Control and Prevention's Advisory Committee on Immunization
Practices (ACIP). |
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Course
Directors
John
G. Bartlett, MD
Professor of Medicine
Department of Medicine
The Johns Hopkins University
School of Medicine
Baltimore, MD
Paul
G. Auwaerter, MD
Associate Professor of Medicine
Clinical Director
Division of Infectious Diseases
The Johns Hopkins University
School of Medicine
Baltimore, MD
Sara
E. Cosgrove, MD, MS
Assistant Professor of Medicine
Division of Infectious Diseases
Director
Antibiotic Management Program
Associate Hospital Epidemiologist
The Johns Hopkins University
School of Medicine
Baltimore, MD |
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GUEST
AUTHOR OF THE MONTH |
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Commentary
& Reviews: |
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Tom
Talbot, MD, MPH
Assistant Professor of Medicine and Preventive
Medicine
Chief Hospital Epidemiologist
Vanderbilt University
School of Medicine
Nashville, TN |
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Guest
Faculty Disclosures
Tom
Talbot, MD, MPH has disclosed that he has
served as a principal investigator for Sanofi-Pasteur.
Unlabeled/Unapproved Uses
The author has indicated that there will be no
reference to unlabeled/unapproved uses of drugs
or products in the presentation.
Program
Directors' Disclosures |
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At
the conclusion of this activity, participants should
be able to:
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Describe
the efficacy of the herpes zoster vaccine in adults
age 60 years and older |
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Discuss
the limitations of therapeutic efficacy of human
papillomavirus vaccines |
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Discuss
the rationale behind recommendations advising
vaccination of all adults against pertussis |
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Describe
the role of hepatitis A vaccine for use as post-exposure
prophylaxis |
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Complete the post-test and course evaluation.
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eInfections
Review is proud to continue its accredited
PODCASTS for 2008. Listen
here. |
In
this audio interview, Dr. Tom Talbot from Vanderbilt
University School of Medicine discusses some of the
vaccines available for adults, specifically, herpes
zoster, HPV, pertussis, hepatitis A, and influenza.
Participants can now receive 0.5 credits per podcast
after completing an online post-test via the links provided
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To learn more about podcasting and how to access this
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please visit
this page. |
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The
institution and comprehensive implementation of routine
childhood immunization against contagious pathogens
can be considered one of the greatest public health
achievements of the past century. In 2006, 95.8% of
children aged 19-35 months had received 3 or more doses
of diphtheria, tetanus toxoid, and acellular pertussis
vaccine (DTaP), 92.9% had been vaccinated against polio,
and 92.4% had received at least 1 dose of the measles-mumps-rubella
(MMR) vaccine.1
In total, 77% of children in this age group had been
fully vaccinated against diphtheria, tetanus, pertussis,
polio, measles, mumps, rubella, Haemophilus influenzae
type b (Hib), hepatitis B virus, and varicella. Routine
childhood immunization has had tremendous effects upon
the incidence of and morbidity due to many of these
infectious diseases. Deaths due to diseases for which
a vaccine was licensed or recommended prior to 1980
(diphtheria, measles, mumps, pertussis, poliomyelitis,
rubella, smallpox, and tetanus) have declined to near
zero, smallpox has been eradicated worldwide, and the
endemic spread of measles, polio, and rubella has been
eliminated in the United States.2
The table below summarizes these data:
It is estimated that vaccination with 7 of the 12 routinely
recommended childhood vaccines (DTaP; tetanus and diphtheria
toxoids; Hib conjugate; inactivated poliovirus; measles,
mumps, and rubella; hepatitis B; and varicella vaccines)
prevents an estimated 33,000 deaths and 14 million cases
of disease in each birth cohort and saves $9.9 billion
in direct and another $33 billion in indirect costs.3
Simply put, routine childhood immunization has had a
remarkable impact on the health of children in the United
States.
The story of immunizations in the adult population,
however, provides a striking contrast. In 2005, only
22.9% of all adults aged 50-64 years, 25.3% of adults
age 18-64 years with a high-risk condition, and 8.9%
of adults age 18-49 years who were household contacts
of high-risk persons, received an influenza vaccination.4
That same year, only 65.7% of adults 65 years and older
reported receipt of pneumococcal vaccine.5
In the past few years, new vaccines have been licensed
for the adolescent and adult population, including vaccines
against pertussis, human papillomavirus (HPV), and varicella.
While traditionally targeting acute contagious infections
(such as measles or polio), some of the newer adult
vaccines address chronic sequelae of infectious diseases,
like cervical neoplasia in the case of the HPV vaccine
and neuropathy in the case of the varicella zoster vaccine.
These new vaccines impact infectious diseases that can
cause substantial morbidity in adults. Reactivation
of varicella zoster virus, whose primary infection results
in chickenpox, causes up to a million cases of herpes
zoster (shingles) in the United States annually, with
risk increasing as age advances.6
HPV causes 6.2 million new infections each year among
persons aged 14 to 44 years of age, and 70% of cervical
cancers are due to HPV types 16 and 18 (which are included
in the currently licensed vaccine).7
The incidence of pertussis, while markedly decreased
following implementation of childhood vaccination, has
climbed in recent years, with an increasing proportion
of cases noted in adolescents and adults due to waning
protection from pediatric vaccination.8
In addition to these novel vaccines, broader recommendations
for the use of hepatitis B vaccine (ie, no longer requiring
acknowledgment of a hepatitis B virus infection risk
factor for adults to receive the vaccine),9
hepatitis A vaccine (ie, for post-exposure prophylaxis),10
and influenza vaccine (ie, the decrease of the target
age for universal vaccination of all adults from 65
to 50 years and older)11
have emerged for adults in recent years. This growing
number of recommended adult vaccines, combined with
the historically low coverage of established adult immunizations,
has created an important challenge for the medical community.
Adult primary care physicians and internists must emulate
the successes noted by our pediatric colleagues and
integrate immunization into routine preventive adult
care. Using vaccination delivery and adherence as a
measure of quality of patient care has also been advocated.12
In addition, a similar infrastructure to assist in the
delivery these vaccines, particularly to the uninsured,
must be provided to ensure complete access.
A complete summary and tables of recommendations for
adult vaccination can be found on the CDC
website.
References
| 1. |
Centers
for Disease Control and Prevention. National,
state, and local area vaccination coverage among
children aged 19-35 months--United States, 2006.
MMWR Morb Mortal Wkly Rep 2007; 56:880-885. |
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| 2. |
Roush
SW, Murphy TV. Historical
Comparisons of Morbidity and Mortality for Vaccine-Preventable
Diseases in the United States. JAMA
2007; 298:2155-2163. |
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| 3. |
Zhou
F, Santoli J, Messonnier ML, et al. Economic
evaluation of the 7-vaccine routine childhood
immunization schedule in the United States, 2001.
Arch Pediatr Adolesc Med 2005; 159:1136-1144. |
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| 4. |
Fiore
AE, Shay DK, Haber P, et al. Prevention and control
of influenza. Recommendations
of the Advisory Committee on Immunization Practices
(ACIP), 2007. MMWR Recomm Rep 2007;
56:1-54. |
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| 5. |
Centers
for Disease Control and Prevention. Influenza
and pneumococcal vaccination coverage among persons
aged > or = 65 years--United States, 2004-2005.
MMWR Morb Mortal Wkly Rep 2006; 55:1065-1068. |
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| 6. |
Kimberlin
DW, Whitley RJ. Varicella-zoster
vaccine for the prevention of herpes zoster.
N Engl J Med 2007; 356:1338-1343. |
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| 7. |
Markowitz
LE, Dunne EF, Saraiya M, Lawson HW, Chesson H,
Unger ER. Quadrivalent
Human Papillomavirus Vaccine: Recommendations
of the Advisory Committee on Immunization Practices
(ACIP). MMWR Recomm Rep 2007; 56:1-24. |
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| 8. |
Kretsinger
K, Broder KR, Cortese MM, et al. Preventing
tetanus, diphtheria, and pertussis among adults:
use of tetanus toxoid, reduced diphtheria toxoid
and acellular pertussis vaccine recommendations
of the Advisory Committee on Immunization Practices
(ACIP) and recommendation of ACIP, supported by
the Healthcare Infection Control Practices Advisory
Committee (HICPAC), for use of Tdap among health-care
personnel. MMWR Recomm Rep 2006;
55:1-37. |
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| 9. |
Mast
EE, Weinbaum CM, Fiore AE, et al. A
comprehensive immunization strategy to eliminate
transmission of hepatitis B virus infection in
the United States: recommendations of the Advisory
Committee on Immunization Practices (ACIP) Part
II: immunization of adults. MMWR Recomm
Rep 2006; 55:1-33; quiz CE1-4. |
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| 10. |
Centers
for Disease Control and Prevention. Update:
Prevention of hepatitis A after exposure to hepatitis
A virus and in international travelers. Updated
recommendations of the Advisory Committee on Immunization
Practices (ACIP). MMWR Morb Mortal Wkly
Rep 2007; 56:1080-1084. |
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| 11. |
Bridges
CB, Winquist AG, Fukuda K, Cox NJ, Singleton JA,
Strikas RA. Prevention
and control of influenza: recommendations of the
Advisory Committee on Immunization Practices (ACIP).
MMWR Recomm Rep 2000; 49:1-38; quiz CE1-7. |
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| 12. |
Poland
GA, Schaffner W. Adult
Immunization Guidelines: A Patient Safety and
Quality-of-Care Issue. Ann Intern Med
2007; 147(10):735-737. Epub 2007 Oct 18. |
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THE
EFFICACY OF A VACCINE AGAINST HERPES ZOSTER AND
POST-HERPETIC NEURALGIA |
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Oxman
MN, Levin MJ, Johnson GR, et al. A
vaccine to prevent herpes zoster and postherpetic
neuralgia in older adults. N
Engl J Med 2005; 352:2271-2284.
(For non-journal subscribers, an additional
fee may apply for full text articles.)
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In
June 2005, the results of one of the largest vaccine
efficacy trials, the Shingles Prevention Study,
were reported. In a randomized, double-blind,
placebo-controlled trial of adults age 60 or older,
the use of a vaccine against zoster (containing
14 times the minimum estimated potency found with
its pediatric counterpart) was studied. Subjects
with a history of varicella (chicken pox) or residence
of at least 30 years in the continental United
States were eligible for enrollment. Immunocompromised
persons, those with chronic pain syndromes, and
persons with a prior history of herpes zoster
(shingles) were excluded. Randomized by study
site and age group (age 60-69 years, and ≥70
years), subjects received either zoster vaccine
or placebo. Subjects were educated regarding the
signs and symptoms of herpes zoster, and were
followed via monthly automated phone calls to
assess for the presence of the disease. Suspected
zoster rashes were evaluated using polymerase
chain reaction (PCR) and culture testing of a
swab from a characteristic lesion. The final determination
of a case of herpes zoster was made by a physician
committee blinded to the subject's treatment assignment.
The primary end point for the study was the burden
of illness due to herpes zoster (a measurement
of pain and discomfort associated with the disease),
while other end points included the incidence
of post-herpetic neuralgia and the incidence of
herpes zoster.
A remarkable 38,546 adult subjects enrolled in
the trial, with 95.3% completing the study for
a mean duration of herpes zoster surveillance
of 3.13 years (no difference between study arms).
Vaccination with the zoster vaccine reduced the
burden of illness due to herpes zoster by 61.1%
(95% confidence intervals [CI], 51.1-69.1%), the
incidence of post-herpetic neuralgia by 66.5%
(95% CI, 51.1-69.1%), and the incidence of herpes
zoster by 51.3% (95% CI, 44.2-57.6%). The zoster
vaccine led to a significantly higher rate of
injection site complaints, but these were generally
mild.
Spurred by the results of the Shingles Prevention
Study, the ACIP recommended that all adults aged
60 years or older receive the zoster vaccine,
regardless of a prior history of shingles.1
Issues such as the cost-effectiveness of vaccination,
reimbursement for the vaccine by third-party payors,
and the timing of vaccination in persons with
a recent history of shingles still must be ascertained
and further defined.
References
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USE
OF A BIVALENT HUMAN PAPILLOMAVIRUS VACCINE IN WOMEN
WITH PRE-EXISITING HPV INFECTION |
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Hildesheim
A, Herrero R, Wacholder S, et al. Effect
of human papillomavirus 16/18 L1 viruslike particle
vaccine among young women with preexisting infection:
a randomized trial. JAMA 2007;
298:743-753.
(For non-journal subscribers, an additional
fee may apply for full text articles.) |
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While
the studies examining the use of quadrivalent human
papillomavirus (HPV) vaccine in HPV-naïve women were
reviewed in last month's issue, this study by Hildesheim
et al highlights an important issue with regards to
HPV vaccines; namely, their effectiveness in women previously
exposed to the HPV types included in the vaccine. In
this trial (a substudy of a larger, randomized, blinded
clinical trial examining the efficacy of a bivalent
HPV vaccine targeting HPV types 16 and 18 in women aged
18 to 25 years in Costa Rica), the impact of vaccination
on viral clearance in women already infected with HPV
was examined. Eligible subjects (n=7,466) were enrolled
and vaccinated with either the bivalent HPV vaccine
or hepatitis A vaccine as a control at 0, 1, and 6 months.
Serum samples for HPV antibody testing (against HPV-16
and HPV-18) and cervical cytology specimens for HPV
DNA testing by PCR were collected at enrollment. Subjects
also underwent follow-up examination at 12 months post-enrollment,
where cervical cytologic evaluation for HPV DNA also
occurred. Subjects with evidence of HPV DNA at enrollment
were eligible for the substudy.
In the substudy, the primary endpoint was HPV clearance
at the 6- and 12-month visits, defined as failure to
detect (at the respective follow-up visits) an HPV type
that was present before vaccination. Investigators also
measured the vaccine efficacy for viral clearance (VEVC),
a measurement of the percentage change in infection
rates observed in the HPV vaccine arm as compared to
the control arm. A total of 2,189 women were eligible
and included in the substudy (1,088 in the HPV vaccine
arm, 1,101 in the control arm). Rates of viral clearance
and VEVC for vaccine-associated genotypes of HPV at
the 6 and 12 month visits are shown in the table below:
Notably, there were no significant differences in viral
clearance or VEVC between the HPV vaccine and control
groups, indicating no therapeutic effect of the bivalent
HPV vaccination in this population. These findings remained
even after stratification for HPV serologic status at
study entry, presence of abnormal cervical cytology
on study entry, level of viral load at study entry,
time since sexual initiation, contraceptive use, smoking
status, and chlamydia/gonorrhea status at study entry.
Unanswered questions remain regarding the use of the
bivalent vaccine in persons already exposed to HPV prior
to vaccination. Is there still a benefit in vaccinating
women infected with HPV who have not been exposed to
all genotypes of HPV included in the vaccine? Other
investigations have shown protection against other HPV
types with use of the quadrivalent vaccine in this population1
thus, it seems likely that investigations with the bivalent
version will produce similar findings.
The findings from this study reinforce those from prior
investigations with the quadrivalent vaccine that showed
no type-specific therapeutic efficacy of HPV vaccination
in subjects with evidence of vaccine-type HPV exposure
prior to vaccination.7
The quadrivalent HPV vaccine is recommended by the ACIP
for routine vaccination of women aged 11 to 12 years
and for catch-up vaccination for women aged 13 to 26
years.7
These recommendations also note that, while vaccination
against HPV before sexual debut is preferred, women
who may have already been exposed to HPV (eg, sexually-active,
those with previously identified HPV on cytologic examination)
should also be vaccinated. Testing women prior to vaccination
via Papanicolaou smear or HPV DNA analysis is not recommended.
References
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ACELLUAR
PERTUSSIS VACCINATION OF ADULTS |
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Ward
JI, Cherry JD, Chang SJ, et al. Efficacy
of an acellular pertussis vaccine among adolescents
and adults. N Engl J Med 2005;
353:1555-1563.
(For non-journal subscribers, an additional
fee may apply for full text articles.) |
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With
the rising incidence of infection due to Bordetella
pertussis (aka, pertussis or "whooping cough")
in adolescents and adults over the past two decades,
there has been a growing interest in methods to prevent
such morbidity in this population.1
Routine pertussis vaccination of infants has been recommended
since the 1940s, with a less-reactogenic acellular vaccine
first licensed for pediatric use in 1991. Vaccination
of infants against pertussis has led to a marked decline
in disease in this population.1
In the Adult Pertussis Trial (APERT), Ward et al examined
the safety and efficacy in the adult and adolescent
population of an acellular pertussis vaccine, which
contained a lower concentration of pertussis antigen
than found in the pediatric vaccine. Persons between
15 and 65 years of age were enrolled in this double-blind
multi-center randomized trial. Subjects were randomly
allocated to receive the acellular pertussis or hepatitis
A vaccine and were followed for 2.5 years with twice
monthly phone calls to ascertain for cough illness (defined
as cough of 5 or more days' duration). Routine serology
for anti-pertussis antibodies was collected periodically
during follow-up. In addition, subjects reporting a
cough illness underwent nasopharyngeal aspiration to
collect specimens for culture and PCR testing as well
as paired acute and convalescent serology analysis for
IgG and IgA antibodies to four key B. pertussis
antigens. A case of pertussis was defined as a cough
illness with confirmatory positive culture or PCR for
B. pertussis or a pre-defined rise in antibody
titers.
A total of 2,781 subjects were enrolled in the study
(1,390 receiving the acellular pertussis vaccine and
1,391 receiving the hepatitis A vaccine control). The
median duration of follow-up of both study arms was
22 months. Of the 2,672 reported cough illnesses, only
10 episodes met the primary case definition for pertussis.
Nine of these cases occurred in the control arm, yielding
an overall vaccine efficacy of 92% (95% confidence interval,
32-99%), which is similar to that found in studies of
pediatric formulations of the vaccine. Pertussis was
a more likely cause of cough illness with prolonged
duration of cough (occurring in 0.7% of cough illnesses
lasting more than 5 days vs 5.7% of cough illnesses
lasting more than 56 days). No vaccine-related serious
adverse events occurred in either arm.
Prompted in part by the results of the APERT investigation,
the ACIP released new recommendations regarding the
use in adults of the newly licensed acellular pertussis
vaccine (which includes tetanus toxoid, reduced diphtheria
toxoid, and acellular pertussis antigens and is designated
as Tdap).1
Specifically, all adults age 19-64 years of age should
now receive Tdap in place of the tetanus diphtheria
(Td) booster if the last dose of Td was ≥10 years
ago (or as indicated for wound care). Intervals less
than 10 years since Td may be used when determining
administration of Tdap, particularly in settings where
there is an increased risk of pertussis or complications
due to B. pertussis infection. In addition,
persons who have close contact with an infant younger
than 1 year should receive Tdap if it has been as short
as 2 years since receipt of the Td booster. Finally,
because of the increased risk of exposure to persons
with pertussis, the ACIP and the Healthcare Infection
Control Practices Advisory Group recommended that all
healthcare workers with direct patient contact receive
a dose of Tdap if it has been at least 2 years since
receipt of Td both to protect themselves and to reduce
transmission of pertussis to their patients.
References
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THE
USE OF HEPATITIS A VACCINE FOR POST-EXPOSURE PROPHYLAXIS |
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Victor
JC, Monto AS, Surdina TY, et al. Hepatitis
A vaccine versus immune globulin for postexposure
prophylaxis. N Engl J Med 2007;
357:1685-1694.
(For non-journal subscribers, an additional
fee may apply for full text articles.) |
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In
a randomized, double-blind, noninferiority trial based
in Kazakhstan, Victor et al compared two methods of
post-exposure prophylaxis (PEP) in household and day-care
contacts of laboratory-confirmed symptomatic cases of
hepatitis A virus (HAV) infection. The study population
consisted of healthy persons aged 2 to 40 years who
were exposed to index cases of HAV infection. Eligible
subjects were randomized to receive either hepatitis
A vaccine or weight-based immune globulin (the traditionally
recommended intervention for prophylaxis) within 14
days after exposure. At randomization, contacts underwent
serologic testing for HAV, and those contacts susceptible
to HAV were evaluated over the next 8 weeks for evidence
of incident hepatitis A infection (ie, serology for
HAV and alanine aminotransferase levels in all subjects;
additional PCR testing of serum and stool specimens
for contacts with positive serology).
A total of 4,524 contacts were randomized to receive
one of the two PEP interventions, while 1,090 contacts
were found to be susceptible to HAV and, therefore,
eligible for follow-up. Symptomatic hepatitis A infection
was noted in 4.4% (25/568) of contacts who received
hepatitis A vaccination, while 3.3% (17/522) of contacts
who received immune globulin developed hepatitis A infection
(relative risk of infection of 1.35; 95% confidence
interval, 0.70-2.67), which met the pre-determined criterion
for noninferiority. While not showing a significant
increase compared with the immune globulin arm, there
were higher rates of clinical and subclinical HAV infections
in subjects who received the vaccine, suggesting a potential
small difference between the two interventions. Vaccination
was well-tolerated, with no reports of unexpected adverse
events.
Based upon this trial, the ACIP, in mid-2007, revised
their recommendations for care of persons recently exposed
to HAV.1
Namely, for healthy persons aged 1 to 40 years, single
antigen hepatitis A vaccine (not the combined hepatitis
A and B vaccine, due to the reduced amount of HAV antigen
in the combined vaccine) is now recommended for PEP.
Immune globulin is preferred for healthy adults over
age 40 years, but these contacts may be vaccinated if
immune globulin is unavailable. For persons younger
than 1 year, immunocompromised patients, and/or patients
with chronic liver disease, immune globulin remains
the preferred method of PEP. Previously, the ACIP had
also recommended that international travelers headed
to areas of high or intermediate HAV endemicity receive
the hepatitis A vaccine. If the planned travel was less
than 4 weeks from the time of vaccination, immune globulin
was also recommended. Based on the results of the above
trial, hepatitis A vaccine alone may be given to healthy
adults age 40 or younger prior to international travel
regardless of their scheduled dates for departure.1
While a long-established method of PEP, the use of immune
globulin has several key concerns, including cost, the
requirement for a large volume of administration, limited
access and availability, inability to provide long-term
immunity, and concerns about transmission of bloodborne
pathogens. This study supports the use of hepatitis
A vaccine as an alternative to immune globulin for PEP
of select healthy contacts to an index case of hepatitis
A.
References
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At
the conclusion of this activity, participants
should be able to:
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Describe
the efficacy of the herpes zoster vaccine
in adults age 60 years and older |
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Discuss
the limitations of therapeutic efficacy
of human papillomavirus vaccines |
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Discuss
the rationale behind recommendations advising
vaccination of all adults against pertussis |
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Describe
the role of hepatitis A vaccine for use
as post-exposure prophylaxis |
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a provider accredited by The ACCME, it is the
policy of The Johns Hopkins University School
of Medicine to require the disclosure of the existence
of any significant financial interest or any other
relationship a faculty member or a provider has
with the manufacturer(s) of any commercial product(s)
discussed in an educational presentation. The
Program Directors reported the following:
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John
G. Bartlett, MD has disclosed that
he has served on the HIV Advisory Board
for GlaxoSmithKline, Abbott, Bristol-Myers
Squibb, Pfizer and Tibotec. He is also on
the Policy Board for Johnson & Johnson.
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Paul
G. Auwaerter, MD has disclosed
that he has served as a consultant for Novartis,
Pfizer, Ortho-McNeil, Schering-Plough, and
Genzyme. He is on the Speakers' Bureau for
Schering-Plough and has also disclosed that
he is a Stock Shareholder for Johnson &
Johnson. |
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Sara
E. Cosgrove, MD, MS has disclosed
that she has received grants or research
support from Merck and served on the Advisory
Boards for Ortho-McNeil, Cadence Pharmaceuticals,
and Theravance/Astellas. |
Guest
Author Disclosures |
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| Disclaimer
Statement — back
to top |
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| The
opinions and recommendations expressed by faculty
and other experts whose input is included in this
program are their own. Use of The Johns Hopkins
University School of Medicine name implies review
of educational format design and approach. Please
review the complete prescribing information of
specific drugs or combination of drugs, including
indications, contraindications, warnings and adverse
effects before administering pharmacologic therapy
to patients. |
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©
2007 JHUSOM and eInfections Review
Created by
DKBmed. |
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Step
3.
Complete the post-test and course evaluation.
Step
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Print out your certificate.
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