The title of this assignment is Integrative Review.

It was completed in NUR 4122

Nursing Research. The specific program outcome that this assignment demonstrates is Program
Outcome #5 - Demonstrate commitment to the nursing profession and lifelong learning. The
purpose of this assignment was to analyze and critique research applicable to professional
nursing practice and apply research to safe, quality, evidence-based professional practice. This
assignment exemplified Program Outcome #5 because it required analyzing and critiquing
research to communicate findings of current research to improve nursing practice. Also,
evidence-based nursing practice is a key tenet of the nursing profession and one must be
committed to lifelong learning and education.

INTEGRATIVE REVIEW

Human Papillomavirus (HPV) Vaccine Efficacy Among Adolescent Females:

An Integrative Review
David Krukiel
Bon Secours Memorial College of Nursing

Abstract

INTEGRATIVE REVIEW

Currently, there are two commercially available human papillomavirus (HPV) vaccines with a
recommended target age group of 11 to 12 year old females for first vaccination. This integrative
review examined four quantitative studies related to HPV vaccination efficacy among the target
age group of 11 to 12 year old adolescent females, and one qualitative study that examined
reasons mothers chose to vaccinate their daughters. Researchers findings from all quantitative
studies supported the efficacy of HPV vaccination among the target age group, and researchers
findings of the qualitative study found that mothers health-related beliefs were the primary
factor in deciding to vaccinate their daughters. Key findings included HPV vaccination
decreased rates of HPV infection, cervical abnormalities, and genital warts (GW), long-term
efficacy of HPV vaccination was predicted to last for up to 20 years, vaccination rates remained
low among the target age group, adolescent females living below the poverty level were less
likely to be vaccinated, and vaccine efficacy was greatest when administered among the target
age group before first sexual intercourse.
Keywords: HPV, vaccine, efficacy, adolescents, girls, human papillomavirus

Human Papillomavirus (HPV) Vaccine Efficacy Among Adolescent Females:

INTEGRATIVE REVIEW

4
An Integrative Review

In 2006, the United States introduced into the routine immunization schedule human
papillomavirus (HPV) vaccination for females aged 11 to 12 years. Prophylactic HPV
vaccination programs have been developed to prevent cervical cancer and other HPV-related
cancers. A key factor in the overall strategy for cervical cancer prevention is offering evidence
of a prophylactic vaccine that provides long term protection and sustained immune response.
Through clinical trials, researchers have demonstrated the effectiveness of HPV vaccination
(Gertig et al., 2013; Griffioen et al., 2012; Leval et al., 2013; Markowitz et al., 2013; Schwarz et
al., 2014). However, research supporting HPV vaccine efficacy in the target age group (11 to 12
year old females) and studies demonstrating long-term efficacy of HPV vaccination need to be
examined. This paper examines and reviews available research on the efficacy of the HPV
vaccine among the target age group for vaccination (adolescent females) and reasons why
mothers chose to vaccinate their daughters. Five articles were reviewed for this paper, which are
referred to in Table 1. All authors adequately introduced the concepts of their study. It is clear in
all articles that there are HPV vaccines available that may prevent infection with HPV and
reduce the risk of HPV related cancers and diseases (Gertig et al., 2013; Griffioen et al., 2012;
Leval et al., 2013; Markowitz et al., 2013; Schwarz et al., 2014). The type of studies and study
designs are provided in Table 1. All studies were quantitative with the exception of Griffioen et
al. (2012). Also, all authors are listed in Table 1 and the reference page. It is clear that the
authors of each study were qualified and knowledgeable in relation to HPV vaccination as their
credentials were provided. All authors writing styles and titles were clear, concise, and avoided
medical jargon except Schwarz et al. (2014). The title and article of Schwarz et al. (2014)
contained medical jargon that may not be understandable to the average reader and non-

INTEGRATIVE REVIEW

healthcare professionals including the use of the word immunogenicity. Titles for each article
are listed in Table 1. All abstracts were clear, well-organized, and provided an adequate
overview of each study.
Background
Currently, there are two commercially available HPV vaccines with a recommended
target age group of 11 to 12 year old females. However, vaccination rates among adolescents
remain low (Griffioen et al., 2012; Markowitz et al., 2013). HPV vaccination prevents against
HPV infection which can cause multiple HPV-related forms of cancer including cervical cancer.
Cervical cancer is the third most common cancer among women worldwide, and at least 70% of
cervical cancer cases are caused by HPV types 16 and 18 (Schwarz et al., 2014). According to
multiple researchers, HPV vaccination is most effective when administered before first sexual
intercourse in the target age group of 11 to 12 year old females (Gertig et al., 2013; Griffioen et
al., 2012; Leval et al., 2013; Markowitz et al., 2013; Schwarz et al., 2014). The purpose of this
integrated literature review was to examine research on the efficacy of the HPV vaccination in
reducing HPV related diseases among the target age group of adolescent females and examine
reasons why mothers chose to vaccinate their daughters. The aim was to provide evidence
supporting or refuting the efficacy of HPV vaccination among the target age group and long-term
efficacy of vaccination. Reasons for why mothers chose to vaccinate their daughters was also
reviewed to possibly determine reasons for low vaccination rates. For this integrative literature
review, a PICO question was developed before beginning the literature search process. The
population for the integrated review was adolescent females aged 10 to 17 years of age. The
intervention was HPV vaccination and the comparison group was unvaccinated adolescent
females. The outcome was efficacy of HPV vaccination in reducing HPV infection and related

INTEGRATIVE REVIEW

diseases including cervical abnormalities, cervical cancer, and genital warts. Also, the long-term
immune response of vaccinated subjects, and mothers decisions to vaccinate their daughters
were considered outcomes for the purpose of this integrative literature review.
Methods
Search strategy
A literature search was conducted using PubMed, and Nursing Reference Center.
Controlled vocabularies relevant to HPV vaccination, efficacy, and adolescent females were
used. Key words used in search are listed in Table 1. Searches were limited to articles with
abstracts and research articles in English. Articles were restricted to a published date from 2009
to 2014. Studies were chosen if the researchers study population included adolescent girls (10
to 17 years) and measured outcomes of HPV vaccination efficacy. Also, a qualitative study was
included to examine reasons why mothers chose to vaccinate their adolescent daughters.
Researchers designs are described in Table 1 and are further discussed in the results section.
Results
After a preliminary review of retrieved articles, twelve articles were selected. However,
for the purpose of this integrated literature review five articles were selected to examine that met
the inclusion criteria related to the PICO question. One qualitative and four quantitative studies
were selected. Griffioen et al. (2012) was a qualitative study utilizing semistructured interviews
resulting in a generic qualitative design (Ryan, Coughlan, & Cronin, 2007). This study was
chosen because the authors examined the relationship between mothers and daughters, and
mothers decisions to vaccinate. This study was important because according to researchers 11 to
12 year old females are the target age group for HPV vaccine efficacy. However, vaccination
rates among the target age group have remained low. All of the studies were non-experimental.

INTEGRATIVE REVIEW

Gertig et al. (2013) and Leval et al. (2013) utilized a retrospective cohort design. Schwarz et al.
(2014) utilized a follow-up cohort design of an initial observer-blinded, randomized trial.
Random sampling was not used in any study. Sampling was strictly purposive sampling to meet
the inclusion criteria of the studies. Dates of publication are listed in Table 1. Sample sizes
varied from small (N=33 adolescent girls) to large (N=2,209,263). Additional sample sizes are
referenced in Table 1. Sample settings varied per research study. Three studies demonstrated the
efficacy of HPV vaccination in the reduction of HPV infection and related diseases such as
genital warts (GW) (Gertig et al., 2013; Leval et al., 2013; Markowitz et al., 2013). Gertig et al.
(2013) and Leval et al. (2013) both utilized regression analysis in their data analysis. Gertig et
al. (2013) analyzed vaccine effectiveness (VE) and hazard ratios (HR) for cervical abnormalities
by vaccination status of females between 12 and 17 years and found a significant reduction in
cervical abnormalities of vaccinated women (any dose) compared with unvaccinated women
utilizing 95% confidence interval (CI). Leval et al. (2013) analyzed vaccine effectiveness
against genital warts and found that the vaccine was 93% effective in girls vaccinated before age
14 years (CI = 73% to 98%). Markowitz et al. (2013) reached the same conclusion as Gertig et
al. (2013) and Leval et al. (2013), but analyzed HPV prevalence data determined by the Linear
Array HPV Assay cervicovaginal swab samples. Markowitz et al. (2013) results were consistent
with the other researchers findings and showed a decline of 56% of HPV infection prevalence
after the introduction of the HPV vaccine. This decrease was among females aged 14 to 19
years. In another study, Schwarz et al. (2014) supported the other quantitative studies and
demonstrated long-term immune protection when vaccinated with the HPV vaccine. Schwarz et
al. (2014) performed data analysis using the statistical analysis system (SAS) version 9.2 to
determine seropositivity rates and geometric mean titers and found in preteen/adolescent girls the

INTEGRATIVE REVIEW

HPV vaccine induced high anti-HPV antibody levels up to 6 years postvaccination. The
antibody levels were predicted to remain above those caused by natural infection for up to 20
years. Schwarz et al. (2014) demonstrated the long-term effectiveness of HPV vaccination in the
target age group, while the other studies did not look at the long-term effect of HPV vaccination.
All authors of the quantitative studies reached the same conclusion and found that HPV
vaccination is most effective when administered to the target age group before first sexual
intercourse (Gertig et al., 2013; Leval et al., 2013; Markowitz et al., 2013; Schwarz et al., 2014).
Also, it was found that HPV vaccination was most effective when females received all three
doses of the vaccine (Gertig et al., 2013; Leval et al., 2013; Markowitz et al., 2013; Schwarz et
al., 2014). The qualitative study by Griffioen et al. (2012) was critical to examine because it
looked at reasons why mothers chose to vaccinate their daughters which could possibly be used
to develop interventions to increase vaccination among the target age group. Griffioen et al.
(2012) study found the primary factors influencing mothers decisions to vaccinate daughters
against HPV were (a) mothers beliefs and experiences; (b) interactions with clinicians, friends,
and family members; and (c) exposure to media reports/marketing (p. 560). Also, according to
Griffioen et al. (2012), a mothers personal health-related beliefs appeared to be the primary
factor influencing her decision to vaccinate her daughter. In addition, Leval et al. (2013) found
that girls were 15 times more likely to be vaccinated before age 20 if they had at least one
university-educated parent. Furthermore, Gertig et al. (2013) and Markowitz et al. (2013) found
that vaccination rates were lower among women living below the poverty level.

Discussion

INTEGRATIVE REVIEW

This integrated review about HPV vaccine efficacy in the target age group of females 11
to 12 years demonstrated five key findings: (1) Researchers provided evidence supporting the
effectiveness of HPV vaccination against HPV infection, cervical abnormalities, and genital
warts, (2) anti-HPV antibody levels were predicted to remain high for up to 20 years supporting
the long-term efficacy of HPV vaccination, (3) HPV vaccine efficacy is greatest when
administered among the target age group before first sexual intercourse, (4) a mothers personal
health-related beliefs was the primary factor influencing her decision to vaccinate, and (5) HPV
vaccination rates among the target age group remained low. Griffioen et al. (2012) provided
novel insights into why vaccination rates may be low and their findings may be used to develop
interventions to increase vaccination rates. A population-based HPV vaccination school program
as demonstrated by Gertig et al. (2013) that reduced cervical abnormalities for vaccinated
women within five years of implementation may be an option to increase vaccination rates.
Since research has demonstrated that HPV vaccination is greatest when administered among the
target age group, further studies should address developing interventions to increase vaccination
rates. Also, vaccination rates were shown to be lower among girls living below the poverty line,
and girls with non-university educated parents. Interventions should be focused at improving
vaccination rates among lower socioeconomic girls and educating mothers on the health benefits
of HPV vaccination since a mothers personal health related beliefs were found to be the primary
factor influencing her decision to vaccinate her daughter (Griffioen et al., 2012).
Limitations
This literature review was limited to five studies that used non-experimental designs and
non-probability sampling, which provide a lower quality of evidence compared to controlled
randomized clinical trials. Also, the findings may not be transferrable and valid to other

INTEGRATIVE REVIEW

10

populations except the populations studied by the researchers due to the lack of randomization.
Further studies could use experimental designs to examine the cause and effect relationship
between HPV vaccination, and the reduction of HPV infection and related diseases. Also,
current research related to this literature review was not abundant, and there were few studies
addressing long-term efficacy of HPV vaccination. In addition, many articles found were not
available for free to review.
Conclusion
This integrative literature review examined HPV vaccine efficacy in the recommended
target age group of adolescent females. Also, it examined why mothers chose to vaccinate their
adolescent daughters. All researchers examined specific populations that included adolescent
females. Sufficient data was found to support the efficacy of HPV vaccination in the target age
group, and it was clear that HPV vaccine efficacy was greatest when administered at the target
age group before first sexual intercourse. The long-term efficacy of HPV vaccination was
predicted to last for up to 20 years. The establishment of school-based vaccination programs
could increase the rate of HPV vaccination. Increased HPV vaccination rates may reduce the
rate of HPV infection and related diseases such as cervical cancer, and genital warts.
Interventions based off of these studies could be used to promote the HPV vaccine and increase
vaccination rates among adolescent girls especially those living below the poverty level.
Implications for future studies should include long-term studies undertaken to support the longterm efficacy of HPV vaccination among the target age group. In addition, implications for
current practice include insuring complete HPV vaccination (3 doses) among adolescent females
before first sexual intercourse.
References

INTEGRATIVE REVIEW

11

Gertig, D.M., Brotherton, J.M., Budd, A.C., Kelly, D., Genevieve, C., & Saville, A.M. (2013).
Impact of a population-based HPV vaccination program on cervical abnormalities: A data
linkage study. BMC Medicine, 11(227), 1-12. doi:10.1186/1741-7015-11-227
Griffioen, A.M., Glynn, S.G., Mullins, T.K., Zimet, G.D., Rosenthal, S.L., Fortenberry, J.D., &
Kahn, J.A. (2012). Perspectives on decision making about human papillomavirus
vaccination among 11- to 12- year-old girls and their mothers. Clinical Pediatrics, 51(6),
560-568. doi:10.1177/0009922812443732
Leval, A., Herweijer, E., Ploner, A., Eloranta, S., Simard, J.F., Dillner, J., Young, C., Netterlid,
E., Sparn, P., & Arnheim-Dahlstrm, L. (2013). Quadrivalent human papillomavirus
vaccine effectiveness: A Swedish national cohort study. Journal of the National Cancer
Institute, 105(7), 469-474. doi:10.1093/jnci/djt032
Markowitz, L.E., Hariri, S., Lin, C., Dunne, E.F., Steinau, M., Mcquillan, G., & Unger, E.R.
(2013). Reduction in human papillomavirus (HPV) prevalence among young women
following HPV vaccine introduction in the United States, National Health and Nutrition
Examination Surveys, 2003-2010. The Journal of Infectious Disease, 208, 385-393.
doi:10.1093/infdis/jit192
Ryan, F., Coughlan, M., & Cronin. (2007). Step-by-step guide to critiquing research. Part 2:
Qualitative research. British Journal of Nursing 16(12), 738-744. doi:
http://dx.doi.org/10.12968/bjon.2007.16.12.23726
Schwarz, T.F., Huang, L.M., Lin, T.Y., Wittermann, C., Panzer, F., Valencia, A., Suryakiran,
P.V., Lin, L., & Descamps, D. (2014). Long-term immunogenicity and safety of the
16/18 AS04-adjuvanted vaccine in 10- to 14-year-old girls. The Pediatric Infectious
Disease Journal, 33(12), 1255-1261. doi:10.1097/INF.000000000000046

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12

Table 1
NUR 4122: Nursing Research
Table of Evidence
Human Papillomavirus (HPV) Vaccine Efficacy Among Adolescent Females
Auth
ors
(Year
)

Title of
Article

Gerti
g et
al.
(2013
)

Impact of
a
Population
-Based
HPV
Vaccinatio
n Program
on
Cervical
Abnormali
ties: A
Data
Linkage
Study

Data
base

Key
word
s
used
in
searc
h
Nursi HPV,
ng
vacci
Refer ne,
ence effic
Cente acy,
r
adole
scent

Resear
ch
Design

Data
Collec
tion

Sub
ject
s

Sam
pling
Meth
ods

Data
Analys
is

Conclusio
n

Quantit
ative
(observ
ational
study
utilizin
ga
retrosp
ective
cohort
design)

Data
for
wome
n ageeligibl
e for
the
HPV
vaccin
ation
progra
m
were
linked
betwe
en the
Victor
ian
Cervic
al
Cytolo
gy
Regist
ry
(VCC
R) and
the
Nation
al
HPV
Vaccin

38,9
56
wo
men
bet
wee
n 12
and
17
year
s of
age
who
had
a
pap
test
reco
rded
on
the
VC
CR.

Nonproba
bility
sampl
ing
(purp
osive
sampl
ing)

Vaccine
effectiv
eness
(VE)
and
hazard
ratios
(HR)
for
cervical
abnorm
alities
by
vaccina
tion
status
betwee
n April
1, 2007
and
Decem
ber 31,
2011
were
calculat
ed
using
proport
ional
hazards
regressi

A
population
-based
HPV
vaccinatio
n program
in schools
significantl
y reduced
cervical
abnormalit
ies for
vaccinated
women
within five
years of
implement
ation with
the greatest
vaccine
effectivene
ss
observed
for the
youngest
women.

INTEGRATIVE REVIEW

13
ation
Progra
m
Regist
er
(NHV
PR) to
create
a
cohort
of
screen
ing
wome
n who
were
either
vaccin
ated
or
unvac
cinate
d.

Griffi
oen et
al.
(2012
)

Perspecti
ves on
Decision
Making
About
Human
Papillomav
irus
Vaccinatio
n Among
11-to 12Year-Old
Girls and
Their
Mothers

Nursi
ng
Refer
ence
Cente
r

Hum
an
papil
loma
virus
,
vacci
ne,
girls,
adole
scent

Qualita
tive
(generi
c
qualitat
ive
design;
semistr
uctured
intervie
ws)

Semist
ructur
ed
intervi
ews
were
condu
cted
with
girls
and
mothe
rs
separa
tely.

on.

Girl
s
(N=
33)
who
had
rece
ived
an
HP
V
vacc
ine
and
their
mot
hers
(N=

Purpo
sive
sampl
ing

Frame
work
analysi
s

This study
provided
novel
insights
into
perspective
s on
decision
making
about HPV
vaccinatio
n among
mothers
and 11- to
12-yearold
daughters,
which can

INTEGRATIVE REVIEW

14
32).

Leval
et al.
(2013
)

Quadrival Pub
ent Human Med
Papillomav
irus
Vaccine
Effectiven
ess: A
Swedish
National
Cohort
Study

HPV,
vacci
ne,
adole
scent
,
girls,
effic
acy

Quantit
ative
(retrosp
ective
cohort
design)

Mark
owitz
et al.
(2013
)

Reduction
in Human
Papillomav
irus (HPV)
Prevalence
Among

HPV,
vacci
ne,
effec
tiven
ess,

Quantit
ative
(crosssection
al
design)

Nursi
ng
Refer
ence
Cente
r

be used in
interventio
ns to
improve
vaccinatio
n rates.
A
Wo Non- Crude
Vaccine
cohort men proba inciden effectivene
of
aged bility ce rates ss was
girls
10
(purp (IRs) of highest in
and
to
osive GW
girls
wome 44
sampl were
vaccinated
n were year ing)
calculat before age
linked s
ed and 14 years.
to
livin
Poisson Young age
Swedi g in
regressi at first
sh
Swe
on
vaccinatio
popula den
analysi n is
tion
bet
s was
imperative
registe wee
used to for
rs to
n
estimat maximizin
identif Janu
e the
g
y
ary
inciden quadrivale
incide 1,
ce rate nt HPV
nt of
200
ratio
vaccine
genital 6,
(IRR)
effectivene
warts
and
betwee ss.
(GW) Dec
n
in
emb
vaccina
relatio er
ted and
n to
31,
partiall
HPV
201
y
vaccin 0
vaccina
ation. (N=
ted or
2,20
unvacci
9,26
nated
3).
women.
HPV
Fem Non- HPV
The
preval ales proba prevale vaccineence
aged bility nce
type HPV
data
14(purp data
prevalence
from
59
osive were
decreased
the
year sampl analyze among

INTEGRATIVE REVIEW
Young
Women
Following
HPV
Vaccine
Introductio
n in the
United
States,
National
Health and
Nutrition
Examinati
on
Surveys,
20032010

Schw

Long-

adole
scent
,
girls

Pub

HPV, Quantit

15
vaccin
e era
(20072010)
and
the
prevac
cine
era
(20032006)
was
collect
ed
during
Nation
al
Health
and
Nutriti
on
Exami
nation
Surve
ys.
HPV
preval
ence
was
deter
mined
by the
Linear
Array
HPV
Assay
cervic
ovagin
al
swab
sampl
es.
Partici

s
old;
415
0
prov
ided
sam
ples
in
200
3200
6,
and
425
3
prov
ided
sam
ples
in
200
7201
0.

ing)

d using
statistic
al
analysi
s
system
(SAS)
(versio
n 9.3,
SAS
Institut
e, Cary,
NC)
and
SAScallable
SUDA
AN
(versio
n 11.0,
RTI,
Cary,
NC).

females
ages 14-19
years
despite low
vaccine
uptake
within 4
years of
vaccine
introductio
n. The
estimated
vaccine
effectivene
ss was
high.

Wo

Non-

Analys

In

INTEGRATIVE REVIEW
arz et
al.
(2014
)

Term
Immunoge
nicity and
Safety of
the HPV16/18
AS04Adjuvante
d Vaccine
in 10- to
14- YearOld Girls

Med

vacci
ne,
effic
acy,
girls

ative
(follow
-up
cohort
design
of an
initial
observe
rblinded
,
random
ized
trial)

16
pants
who
had
receiv
ed 3
HPV
vaccin
e
doses
at 1014
years
of age
in the
initial
study
were
invite
d to
contin
ue
follow
up for
up to
10
years
postva
ccinati
on.
AntiHPV
antibo
dy
titers
were
measu
red by
enzym
elinked
immu
nosorb
ent

men
(N=
505)
who
parti
cipa
ted
in
the
initi
al
rand
omi
zed
stud
y
and
agre
ed
to
cont
inue
follo
wup
for
up
to
10
year
s
post
vacc
inati
on.

proba
bility
(purp
osive
sampl
ing)

es were
perfor
med
using
statistic
al
analysi
s
system
(SAS)
version
9.2 to
determi
ne
seropos
itivity
rates
and
geomet
ric
mean
titers.

preteen/ad
olescent
girls, the
HPV
vaccine
induced
high antiHPV
antibody
levels up
to 6 years
postvaccin
ation.

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17
assays
at
yearly
visits.