Vaccine 30 (2012) 3546–3556

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Vaccine
journal homepage: www.elsevier.com/locate/vaccine

Factors associated with HPV vaccine uptake in teenage girls: A systematic review
Sharon J.M. Kessels a,b , Helen S. Marshall a,c,d , Maureen Watson e , Annette J. Braunack-Mayer a ,
Rob Reuzel b , Rebecca L. Tooher a,∗
a
Discipline of Public Health, School of Population Health and Clinical Practice, The University of Adelaide, Adelaide, Australia
b
Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
c
Vaccinology and Immunology Research Trials Unit, Women’s and Children’s Hospital, Women’s and Children’s Health Network, Adelaide, Australia
d
Discipline of Paediatrics, School of Paediatrics and Reproductive Health, University of Adelaide, Adelaide, Australia
e
Immunisation Branch, SA Health, Citi Centre Building, 11 Hindmarsh Sq, Adelaide, Australia

a r t i c l e i n f o a b s t r a c t

Article history: Background: Since 2006 Human papillomavirus (HPV) vaccination has become available to adolescent
Received 23 December 2011 girls and women in an increasing number of countries, to protect against the virus causing cervical
Received in revised form 7 March 2012 cancer. The vaccine series is offered in three doses over 6 months, and this study aimed to identify factors
Accepted 20 March 2012
associated with initiation and/or completion of the 3 dose series in (pre-) adolescent girls. Previous studies
Available online 3 April 2012
have considered intention to vaccinate rather than actual vaccination uptake.
Methods: A systematic search of Medline, Medline in process, Embase and CINAHL, from 2006 to March
Keywords:
2011 for articles related to HPV-vaccine uptake among adolescent girls and factors potentially associated
Human papillomavirus
Immunization
with uptake yielded 25 studies.
Vaccine Results: The majority of studies were surveys or retrospective reviews of data, only 5 studies reported
Systematic review data on program completion. Most were conducted in the United States (20/25). Higher vaccine uptake
Adolescent health was associated with having health insurance, of older age, receipt of childhood vaccines, a higher vaccine
Health behaviour related knowledge, more healthcare utilization, having a healthcare provider as a source of informa-
tion and positive vaccine attitudes. In US settings, African American girls were less likely to have either
initiated or completed the three dose vaccination series.
Conclusions: HPV vaccination programs should focus on narrowing disparities in vaccine receipt in ethnic
and racial groups and on providing correct information by a reliable source, e.g. healthcare providers.
School-based vaccination programs have a high vaccine uptake. More studies are required to determine
actual vaccine course completion and factors related to high uptake and completion, and information
from a broader range of developed and developing settings is needed.
© 2012 Elsevier Ltd. All rights reserved.

1. Background
Human papillomavirus (HPV) is a sexually transmitted infec-
tion that is a necessary (but insufficient) cause of 99% of all cervical
cancer cases [1]. Two HPV vaccines are available, Cervarix® and
Gardasil® [2,3], which are the first vaccines directed at the pre-
vention of (cervical) cancer [4]. Cervarix® , a bivalent HPV vaccine,
targets types 16 and 18, responsible for nearly 70% of all cervical
cancer cases, while Gardasil® , a quadrivalent vaccine, also targets
types 6 and 11, which cause nearly 90% of anogenital warts. Clinical
∗ Corresponding author at: Discipline of Public Health, MAIL DROP DX 650 550,
School of Population Health and Clinical Practice, The University of Adelaide SA 5005,
Australia. Tel.: +61 8 8313 1316; fax: +61 8 8303 3339.
E-mail addresses: S.J.M.kessels@student.ru.nl (S.J.M. Kessels),
helen.marshall@adelaide.edu.au (H.S. Marshall), maureen.watson@health.sa.gov.au
(M. Watson), annette.braunackmayer@adelaide.edu.au (A.J. Braunack-Mayer),
r.reuzel@ebh.umcn.nl (R. Reuzel), rebecca.tooher@adelaide.edu.au (R.L. Tooher).
trials showed that both products are safe and well tolerated with
only minor adverse reactions [3]. Both vaccines are also nearly 100%
efficacious against pre-cancerous lesions caused by subtypes 16
and 18 in a naive population. A systemic immune response has been
demonstrated at least 5 years post-vaccination [3,5,6]. Cervarix®
and Gardasil® both require three doses to be delivered intramus-
cularly at intervals of 0, 2 and 6 months [2]. Little is known about
the consequences of delayed doses or incomplete vaccination on
the efficacy of the HPV-vaccine.
In 2006, the United States was the first country to license the
HPV vaccine for females aged 9–26, delivered largely through pri-
mary care providers and funded either through private health
insurance, or for uninsured or underinsured girls through the Vac-
cines for Children program. The US Centres for Disease Control
recommend HPV immunization for girls and boys aged 11–12 years
at the time of their regular preventive care visit, and for women
aged 13–26 years if they have not previously received the HPV
vaccine [7,8]. HPV vaccination of adolescent girls (ideally before

0264-410X/$ – see front matter © 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.vaccine.2012.03.063
 S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556
Table 1
HPV-vaccination coverage rates in different countries [10,63–65].
Country Target age group
Luxembourg 12
France 14
Norway 12
US 13–17
Netherlands 12
Italy 11
Denmark 12
Australia 12
UK 12
Portugal 13
they become sexually active) is currently recommended in many
developed countries, and nationally or regionally funded vaccina-
tion programs for HPV are common [5]. Coverage rates vary widely
[9,10], (Table 1) and programs differ depending on how the health
care system is organized. In some countries vaccination programs
are offered through schools (e.g. Australia, UK) whereas in other
countries immunizations are provided in local health clinics, or
through primary care (e.g. the United States).
In order to maximize coverage of HPV vaccine it is important to
understand which factors influence uptake among (pre-)adolescent
girls. (Systematic) reviews [11–14] have identified predictors of
HPV-vaccine acceptability and decision making. However, to date,
these reviews have primarily included studies with an ‘intention to
vaccinate’ outcome. As vaccination programs for adolescent girls
have been implemented since 2006, data has become available
about the coverage for HPV vaccination, enabling an evaluation of
factors influencing actual vaccination coverage rather than inten-
tion to vaccinate.
Therefore this study aims to evaluate factors associated with
the success of HPV vaccination programs for (pre-)adolescent girls,
where success is measured by either vaccine initiation and/or
completion, through a systematic review of the peer-reviewed lit-
erature.
2. Methods
2.1. Search strategies
Medline, Medline in process, Embase and CINAHL were searched
by two researchers from 2006 to the 7th of March 2011. The search
terms were papillomavirus infections, human papillomavirus or
HPV AND vaccines or papillomavirus vaccines AND adolescent,
child or girl* AND accept*, aware*, attitude*, belief*, behave*, deci-
sion, decide, intent*, know*, perceived*, percept*, risk*, sever*,
uptake*, effectiveness, coverage, vaccination, mass vaccination,
decision making or perception. The reference lists of all included
studies were searched for any additional studies not identified via
the main search (pearling).
2.2. Inclusion and exclusion criteria
We included articles that reported data on HPV vaccination
coverage in girls aged 9–18 years, and at least one of the factors
associated with it and could include surveys, comparative studies
(including randomized controlled trials) and qualitative data. We
excluded modeling studies, cost-effectiveness studies, reviews and
opinion pieces; studies reporting HPV vaccination in boys; studies
which included women aged over 18 years; and where the study’s
main focus was cervical cancer screening and not HPV vaccination.
We only included studies reported in the English language.
3547
Coverage (3 doses) Delivery method
17% (2009) Health care providers (free of charge)
24% (2008) Health care providers (co payment basis)
30% (2010) School based
32% (2010) Health care providers
45% (2009) Health care providers (free of charge)
56% (2009) Health care providers (free of charge)
58% (2010) Health care providers (free of charge)
64–80% (2009) School based (free of charge)
80% (2009) School based (free of charge)
81% (2009) School based (free of charge)
2.3. Data extraction
Data were extracted into a prespecified data extraction form by
one researcher and checked by a second.
2.4. Data analysis
No data were suitable for statistical pooling or meta-analysis.
Instead, data were narratively synthesized and tabulated by
outcome separately for studies reporting vaccine initiation and
completion. Unless otherwise stated, all results from multivariate
analyses are adjusted according to factors stated in the accompa-
nying tables for each outcome.
2.5. Critical appraisal
Included studies were critically appraised to identify factors
which may have introduced bias or limited the generalizability
of the results, including methods of selecting groups, adequacy of
adjustment for confounding in correlational analysis, completeness
of the dataset and risk of misclassification bias, according to the
methods suggested by the National Health and Medical Research
Council (Australia) and the National Institute for Health and Clinical
Excellence (UK) [15,16].
3. Results
The search resulted in 66 potentially eligible abstracts which
were assessed against the inclusion criteria by obtaining the full-
text article. We identified 33 relevant articles representing 25
unique studies, after multiple publications from the same study
were identified (Fig. 1).
3.1. Study characteristics
Of these 25 included studies, 23 studies focused primarily on fac-
tors that influenced initiation of the vaccination program and two
studies reported factors primarily associated with the completion
of the HPV-vaccination program, i.e. receiving all three doses of the
HPV-vaccine. Four studies [17–20] reported factors associated with
initiation and completion of the regimen. The majority of included
studies (20/25) were conducted in the United States. Three of the 25
included studies were conducted in a school-based setting [21–23].
Sample size ranged from 52 to 384,869 (median 889): 22/25 (88%)
studies had a sample size over 100 and nearly half (48%) exceeded
1000. Most 14/25 (56%) of the included studies were surveys, the
rest were retrospective reviews of data. All but one study used a
cross-sectional design. Brewer et al. [24] used a longitudinal design
in which the initial sample of girls were followed up after 12–18
months to determine which factors may have influenced the deci-
sion to initiate the vaccination series in the interim. In 9/15 (60%) of
 3548
Table 2
Included studies and selected demographic characteristics.

Author N Risk of Study setting Response Uptake Girl’s age White (%) Black (%) Hispanic/ Unknown (%)
biasc rate (%) rate (%) (years) other (%)

Brewer et al. [24,66–68]d US 650–889 L Primary care and local health clinics 73 36 10–17 56 35 9 0
Chao et al. [18,28,43]d US 179,580 L Primary care and local health clinics NA 37 9–17 18 7 30 45
Cook et al. [19] US 167,082 L Primary care and local health clinics NA 9 11–18 28 39 25 9
Dempsey et al. [20] US 10,082 L Primary care and local health clinics NA 28 9–18 73 14 NR 13
Ogilvie et al. [22] Canada 2025 L School- based (British Columbia) 50 65 ±11 NR NR NR 100
Reiter et al. [32] US 617 L Primary care and local health clinics 61 31 10–17 68 20 12 0

S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556

Pruitt and Schootman [31] US 1709 L–M Primary care and local health clinics NA 34 13–17 71 9 20 0
Agius et al. [21]b Australia 2926 M School-based 86 86 14–20 NR NR NR 100
Allen et al. [30] US 476 M Primary care and local health clinics 67 19 9–17 36 35 29 0
Caskey et al. [37] US 412 M Primary care and local health clinics 54 30 13–17 61 13 26 0
Cates et al. [40] US 696 M Primary care and local health clinics NA 31 10–17 NR NR NR 100
CDC [17] US 9621 M Primary care and local health clinics 58 44 13–17 NR NR NR 100
McCave [33]b US 227 M Primary care and local health clinics 15 36–57 9–17 NR NR NR 100
Neubrand et al. [44]a US 352 M Primary care and local health clinics NA 58 <21 59 21 19 0
Rand et al. [29]b US 430 M Primary care and local health clinics >90 59 11–17 51 31 18 0
Roberts et al. [23,41,42,69]d UK 2817 M School- based NA 71 12–13 91 1 8 0
Rondy et al. [36] Netherlands 384,869 M Local health clinics NA 50 12–17 NR NR NR 100
Rosenthal et al. [38] US 153 M Primary care and local health clinics 83 26 11–17 34 39 27 0
Rouzier and Giordanella [34]b France 77,744 M Local health clinics NA 18 14–23 NR NR NR 100
Staras et al. [35] US 237,015 M Primary care and local health clinics NA 19 9–17 NR 33 NR 67
Widdice et al. [45]a US 3297 M Primary care and local health clinics NA 28 9–26 29 67 NR 4
Mathur et al. [39] US 155 M–H Primary care and local health clinics 89 38 12–20 NR NR NR 100
Dempsey et al. [25] US 52 H Primary care and local health clinics 12 64 11–17 NR NR NR 100
Gerend et al. [26] US 82 H Primary care and local health clinics NA 47 9–17 71 20 4 6
Yeganeh et al. [27] US 95 H Primary care and local health clinics NA 37 11–17 NR NR 91 9

L – low, M – moderate, H – high.

a
Studies only about factors influencing completion of the HPV vaccination program, uptake rate is completion rate.
b
Four studies did not meet the strict age definition in our inclusion criteria, as each may have included some girls who were over 18 years old. However, we decided to include these studies since we judged the impact on
results would be minimal. Agius et al. [21] and McCave [33] only included secondary school girls, Rouzier and Giordanella [34] included girls up to 23 but reported results by age group so that the results for older women could
be separated from younger girls. One study [45] included women aged 9–26 but since only 5.6% (184/3297) participants were aged over 18 we judged the impact on the results would be minimal.
c
Risk of bias.
d
Studies reported in multiple publications: throughout review will be referred to as: Brewer et al. [24], Chao et al. [28] and Roberts et al. [23]. References are given in this table to all papers reporting the outcomes of the study.
 S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556
Fig. 1. Flowchart included studies.
the studies, more than 50% of the sample was Caucasian. Only one
study included a sample in which more than 50% of participating
girls identified as Black (Table 2).
3.2. Critical appraisal
We judged that most of the included studies were at moder-
ate risk of bias with some mainly smaller studies judged to be at
high risk of bias [25–27]. Table 2 shows the risk of bias category
(L – low, M – moderate, H – high) assigned to each included study.
Methodological problems included selection bias introduced by the
sampling strategy, variation in reported outcomes and variability in
outcome definition and measurement. The reporting of vaccination
coverage rates varied considerably, e.g. reported by caregivers, by
reimbursement data or by hospital data, introducing the possibility
of misclassification bias. There was little consistency in the factors
controlled in multivariate analysis and potentially important con-
founding factors such as race, girls age, and socioeconomic status
were not consistently controlled, potentially limiting the validity
of the study findings. Some studies also lacked sufficient statistical
power given their small samples sizes to identify the independent
influence of some of the factors controlled for, whereas a number of
the very large studies may have been able to detect statistically sig-
nificant associations which may not be clinically relevant. Finally,
most of the included studies were conducted relatively soon after
the start of the vaccination program and it is possible that reported
vaccination rates are lower than has been subsequently achieved
in these programs.
3.3. Factors associated with vaccine initiation
3.3.1. Race/ethnicity
In two large studies [19,28], Black (and Asian [28]) girls were sig-
nificantly less likely to initiate the vaccination program compared
with Caucasian and Hispanic girls. However, in one study [20] Black
and Caucasian girls were more likely to initiate the vaccination pro-
gram than other girls, and in a second study [29] Hispanic girls
were significantly more likely to refuse the HPV vaccination than
Caucasian girls (adjOR 5.88, 95% CI 1.0–34.6). No other significant
3549
differences in rates of vaccine initiation based on ethnicity or race
were detected in any of the other studies [23,30–32] (Table 3).
3.3.2. Girls’ age
In 10/14 studies higher vaccination rates were reported among
older girls [17,20,26,28,30–35], although four studies reported that
the vaccination rate decreased again from the age of 17 years
[19,24,28,34]. Two studies [19,24] reported that the highest HPV-
vaccination rates were found among 13–15-year-old girls, whereas
another study reported the highest uptake among 13 and 14-year-
old girls, with a decrease from age 15 [36] (Table 4).
3.3.3. Area of residence
No significant difference in vaccine initiation by geographic
region was detected in two studies [29,37], although in one of
these studies [29] vaccine refusal rates differed significantly by
residential location in unadjusted analyses, with 23% of the sub-
urban and 10% of the urban parents refusing HPV-vaccination
for their daughters. In two studies [32,35], vaccine initiation was
higher among teenage girls living in urban areas compared with
rural areas. In the third study [36], a shorter distance between
home and the vaccination center was significantly associated with
higher vaccine uptake, and geographic region was found to influ-
ence vaccine uptake in multivariate analysis in the fourth study
[19] (Supplementary file 1).
3.3.4. Parental education level and family income
Five studies [26,27,30,31,38] reported no significant associa-
tion between parents’ education and daughter’s HPV-vaccination
uptake. One study [24] found higher vaccine uptake in girls of par-
ents with a college education compared to a high school education
(adjusted OR = 1.69, 95% CI = 1.04–2.73). However, in another study
[22] higher uptake levels were associated with lower parental edu-
cation levels (college vs. high school: adjOR 0.6, 95% CI = 0.5–0.8;
postgraduate degree vs. high school: adjOR 0.6 95% CI = 0.4–0.9). In
three (small) studies no significant correlation between parental
income and vaccine initiation was detected [27,32,37]. However,
in two larger studies lower parental income was found to be a sig-
nificant predictor of vaccine initiation [17,31]. One small study of
82 participants [26], reported the opposite (Supplementary file 2).
3550 S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556

Table 3
Race/ethnicity as a predictor of vaccine initiation and completion.

Outcome Caucasian Black Hispanic Asian Am. Indian Other

Initiation OR/RR (95% CI)

Allen et al. [30]e N = 476 (OR) 1.0 0.87 (0.26–2.86) 1.46 (0.54–3.98) NR NR NR
Chao et al. [28]e N = 179,580 (RR) 1.0 0.93 (0.90–0.95) 1.04 (1.03–1.06) 0.93 (0.91–0.96) NR 0.87 (0.85–0.89)
Cook et al. [19]f n = 167,082 (OR) 1.0 0.87 (0.83–0.92) 1.32 (1.26-1.39) NR NR 1.04 (0.96–1.13)
Dempsey et al. [20]g n = 10,082 (OR) 1.0 1.06 (0.91–1.24) NR NR NR 0.78 (0.66–0.93)
Roberts et al. [23]a , h n = 2817 (OR) 1.0 0.70 (0.20–2.20) NR 0.7 (0.5–1.1) NR 0.40 (0.20–1.2)
Pruitt and Schootman [31]h n = 1709 (OR) 1.0 0.85 (0.58–1.25) 1.04 (0.58–1.88) NR NR 0.90 (0.81–1.01)
Reiter et al. [32]i n = 617 (OR) 1.0 1.03 (0.57–1.88) NR NR NR 0.83 (0.42–1.64)

Completion OR/RR (95% CI)

Chao et al. [18]j N = 24,676 (RR) 1.0 0.70 (0.64–0.77) 0.88 (0.83–0.93) 0.96 (0.87–1.05) NR 0.92 (0.88–0.96)
Cook et al. [19]k N = 167,082 (OR) 1.0 0.56 (0.50–0.62) 0.94 (0.83–1.06) NR NR 0.96 (0.80–1.14)
Widdice et al. [45]l N = 3297 (OR) 1.92 (1.59–2.27) 1.0 NR NR NR NR
1.35 (0.83–2.22) NR NR NR NR 1.0

Initiation rates % (95% CI) (n/N)

Chao et al. [28] n = 179,580 27.7 (9255/33450) 23.3 (3797/15011) 29.2 (15987/54785) 28.7 (2749/9595) NR 23.9 (8500/35509)
Staras et al. [35]b n = 98,880 17.3 16.7 22.5 NR NR NR
CDC [17] n = 9621 43.9 (41.8–46.1) 44.6 (29.9–49.5) 45.5 (40.3–50.8) 41.5 (29.5–54.5) 52.3 (39.0–65.2) NR
Dempsey et al. [20] n = 10,082 28 (n = 2069) 34 (n = 463) NR NR NR 25 (n = 323)
Reiter et al. [32] n = 617 31.6 (150/450) 32.3 (26/89) NR NR NR 27.6 (22/78)
Caskey et al. [37] n = 412 33 (N = 252) 28 (N = 55) 21 (N = 69) NR NR 32 (N = 36)
Yeganeh et al. [27] n = 95 NR NR 47.9% (35/73) NR NR NR

Completion rates % (95% CI)

CDC [17] N = 9621 29.1 (27.3–31.0) 23.1 (19.1–27.6) 23.4 (19.7–27.6) 22.1 (14.7–31.8) 29.6 (20.0–41.4) NR
Neubrand et al. [44]c N = 352 69.1 48.6 38.8 NR NR NR
Widdice et al. [45]d N = 3297 37.0 23.8 NR NR NR 27.0

Completion rate (% Eligible girls vaccinated)

Dempsey et al. [20]c N = 10,082 dose 2 82 60 NR NR NR 76
dose 3 77 61 NR NR NR 71
a
Adjusted for imputation.
b
n as it was reported for race (not equivalent to study n).
c
P < 0.0001.
d
P < 0.001.
e
Adjusted for age, US Census tract educational level and household income, health care coverage, primary care provider characteristics, health care utilization and immune
related medical conditions.
f
Adjusted for geographic region, Medicaid plan type, month of vaccination, age and daughter’s sexual activity.
g
Adjusted for age, insurance, medical specialty and visit type.
h
Adjusted for age, household income, parent education, parent insurance.
i
Unadjusted ORs.
j
Adjusted for age and length of health care membership.
k
Adjusted for geographic region, Medicaid plan type, month of vaccination, age, daughter’s sexual activity.
l
Adjusted for insurance, DMPA vaccination and months since vaccine available.

3.3.5. Vaccination history
HPV vaccine initiation was positively associated with meningo-
coccal vaccination in two studies (Adjusted OR = 2.50, 95%
CI = 1.55–4.01 [32], and adjusted OR = 2.27, 95% CI = 1.60–3.23 [24]),
MMR vaccination in three studies [22,23,36] and influenza vaccina-
tion in one study (RR = 1.29, 95% CI = 1.18–1.22) [28]. No significant
association between receipt of any other childhood vaccine (DPT
(diphtheria, pertussis, tetanus), Hib, polio, DT (diphtheria, tetanus))
was detected in one study [23], although another study reported
that receiving all childhood vaccinations was a positive predictor
for HPV-vaccine initiation (adjusted OR = 1.7, 95% CI = 1.1–2.5) [22]
(Supplementary file 3).
3.3.6. Health care utilization
In four studies a preventive care visit in the past six months
(adjusted OR = 7.31, 95% CI = 2.00–26.8) [37] or twelve months 5.09,
95% CI = 2.43–10.67 and 7.24 [22], 95% CI = 3.55–14.78 [31], or com-
pared to problem focused health care visits (adjusted OR = 5.18, 95%
CI = 4.64–5.79) [20] was a significant predictor of vaccine initiation.
3.3.7. Health insurance status
Two studies [20,31] found that girls with health insurance were
more likely to be vaccinated. One of these studies [20] reported that
vaccine initiation was only more common among those with pub-
lic health insurance, compared to no health care coverage. Three
studies reported no significant difference in initiation rate by health
insurance status [27,29,32]. In one study, parents that believed that
their daughters insurance would cover the HPV-vaccination, were
no more likely to have initiated the vaccine series than parents
that did not have this belief [24]. Duration of enrolment (in the
insurance program) was associated with vaccine initiation in two
studies, with longer enrolment being a predictor for initiating the
vaccine series [19,35] (Table 5).
3.3.8. Beliefs, attitudes and intentions
Intention to vaccinate was found to be a significant predictive
factor for the initiation of the HPV-vaccination program (adjusted
RR = 2.04, 95% CI = 1.16–3.95) in one study [24]. Positive parental
attitudes toward vaccination were found to predict vaccine initia-
tion in two studies [22,30], with, parental concerns about vaccine
safety and side effects negatively predictive of vaccine initiation in
three studies [26,27,29]. Although four studies considered the pos-
sible effect of HPV vaccination on undesirable behaviors such as
early initiation of sexual activities [22,24,26,30], only one of these
studies [22] found this to be a predictor of vaccine refusal (adjusted
OR = 5.1, 95% CI = 3.9–6.7) (Supplementary file 4).
3.3.9. Knowledge
Girls who had been vaccinated had a significantly higher
knowledge score about HPV, HPV-vaccination and cervical
 S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556 3551

Table 4
Girls’ age as a predictor of vaccine initiation and completion.

Outcome 9–10 11–12 13–15 15–17 16–18 17

Initiation OR/RR (95% CI)

Brewer et al. [24]l N = 650–889 (OR) NR 1.0 2.31 (1.32–4.04) NR 2.04a (1.21–3.44) NR
Chao et al. [28]m N = 179,580 (RR) 0.45 (0.44–0.46) 1.0 1.17b (1.15–1.18) 1.14b (1.12–1.16) NR 0.94 (0.91–0.96)
Cook et al. [19]n n = 167,082 (OR) NR 1.0 1.39 (1.33–1.46) NR 0.84 (0.80–0.88) NR
Dempsey et al. [20]o n = 10,082 (OR) 0.03 (0.02–0.05) 1.0 1.44 (1.25–1.65) NR 1.92c (1.66–2.23) NR
Pruitt and Schootman [31]p n = 1709 (OR) NR NR 1.0d 1.24 (1.02–1.50) NR NR
Reiter et al. [32]q n = 617 (OR) NR 1.0e 2.03 (1.12–3.67) NR 3.21e 1.76–5.86) NR
Rondy et al. [36]r n = 384,869 NR 1.06f (1.03–1.08) 1.11f (1.09–1.14) 1.10f (1.08–1.12) 1.0f NR

Initiation rates % (95% CI) (n)

Brewer et al. [24]l n = 650–889 NR 24.0 (25) 39.0† (75) NR 38.0a , † (131) NR
CDC [17] n = 9621 NR 37.1g (33.5–40.9) 40.6g (36.8–44.6) 46.0g (42.1–50.0) 49.9g (45.4–54.4 0 47.1 (43.1–51.2)
Dempsey et al. [20] n = 10,082 2.0† 32.0† 38.0† NR 39.0c , † NR
McCave [33] n = 227 24.7–35.5h NR 35.9–57.1h NR NR NR
Reiter et al. [32]q n = 617 NR 18.8e 33.2 NR 45.2e NR
Rouzier and Giordanella [34] n = 77,774 18.0i , † 30.0i , † 32.0i , † 29.0i , † 26.0i , † 16.0i , †
Staras et al. [35] n = 98,880 1.6, 3.8j 11.7j , 19.7j 22.9j , 21.6j 21.0j 18.6j 15.7

Age at vaccination Girls age mean (SD)

Vaccinated Not vaccinated p Value

Chao et al. [28] n = 179,580 13.8 (2.1) 13.0 (2.7) <0.01 – – –

Gerend et al. [26] n = 82 13.7 (1.8) 11.9 (2.2) <0.05 – – –
†
p < 0.01.
a
Age group 16–20.
b
Age groups: 13–14, 15–16, 17.
c
Age group: 16+.
d
Age group 13–14.
e
Age groups: 10–12; 16–17.
f
Age groups: 12, 13, 14, 15, 16.
g
Age groups: 13, 14, 15, 16, 17.
h
Age groups: 9–12, 13–17.
i
Age groups: 14, 15, 16, 17, 18, 19.
j
Age groups: 9, 10, 11, 12, 13, 14, 15, 16, 17.
l
Adjusted for preventive care visit in the last year, received meningococcal vaccine and education level.
m
Adjusted for provider medical center, girls’/women’s length of health plan membership, age, race, US Census tract educational level and household income, Medi-Cal
enrolee, primary care provider characteristics, health care utilization and immune related medical conditions.
n
Adjusted for geographic region, Medicaid plan type, month of vaccination, race, daughter’s sexual activity.
o
Adjusted for race, insurance, medical specialty and visit type.
p
Adjusted for race/ethnicity, household income, parent education, parent insurance.
q
Adjusted for regular healthcare provider, preventive check up in the last 12 months, received meningococcal vaccine, parent characteristics, urbanicity (and other
characteristics of county of residence).
r
Adjusted for implementation aspects and dates of vaccination.

cancer, compared to non-vaccinated girls in three studies
[21,37,39]. Two other studies [26,30] reported that caregivers of
vaccinated girls also had a better knowledge about HPV (vaccines),
compared to parents of girls that were not vaccinated (adjusted
OR = 1.79, 95% CI = 1.22–2.84 [30]), although both studies had small
sample sizes with limited or no control over potential confounding
factors. A sixth study [24] that controlled for parental characteris-
tics, social influences and sources/quality of information reported
the level of knowledge had no significant effect (adjusted RR = 1.49,
95% CI = 0.96–2.30).
3.3.10. Sources and quantity of HPV-information
Vaccine uptake was positively associated with having heard
about the vaccine from a healthcare provider in four studies
[24,37,39,40]. Higher uptake was also found if the information
source was a newspaper, family, friends or a brochure, with
the uptake also higher, compared to other information sources
[24,39,40]. Parental satisfaction with the amount and quality of
information was significantly associated with vaccine uptake in
three studies, with vaccine refusal linked to dissatisfaction with
information. [24,41,42].
HPV-vaccine course in two studies [26,37], but was not significantly
associated in a third study [24].
3.3.12. Other factors
Family history of sexually transmitted infection (STI) or HPV-
related disease was positively associated with HPV vaccination in
two studies [37,48], but no significant association was detected in a
third [24,38,43]. In one study a traditional family composition was
associated with vaccine initiation [22], however, two other stud-
ies found no significant association [26,27]. One study [19] found
sexual activity positively predicted vaccine initiation (OR = 1.19,
95% CI = 1.15–1.24). However, a second study [38] found no sig-
nificant association with other sexual activity factors (such as the
mothers’ age of sexual initiation, the daughter’s dating status, her
anticipated age of sexual initiation, the number of sexual topics
discussed, the mother’s comfort with sexual conversations and the
mother’s sexual values).
Other remaining factors were not included in this review but
are summarized in Supplementary file 5.
3.4. Factors associated with vaccine completion

3.3.11. Physician recommendation and specialty 3.4.1. Race/ethnicity

A doctor’s recommendation, or having discussed the vaccine Race/ethnicity was reported in six studies [17–20,44,45]. In
with a healthcare provider was a positive predictor for initiating the these six studies, Caucasian girls were most likely to complete
3552 S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556

Table 5
Health insurance as a predictor of vaccine initiation and completion.

Outcome Insurance No insurance Missing

Private Public

Initiation OR (95% CI)

Dempsey et al. [20]c 0.52 (0.45–0.59) 1.0 0.47 (0.26–0.85) NR
Pruitt and Schootman [31]d 1.0 0.48 (0.34–0.69) 0.45 (0.10–2.01)
Rand et al. [29]e 1.0 0.6 (0.2–1.9) NR NR
Reiter et al. [32] 2.43 (0.71–8.30) 1.0 NR

Completion OR (95% CI)

Widdice et al. [45]f 1.16 (0.97–1.38) 1.0 NR NR
NR 2.08 (1.16–3.70) 1.0 NR

Initiation rate % (n)

Dempsey et al. [20]a 27% 35% 24% NR
Reiter et al. [32] 32.10% 16.30% NR
Yeganeh et al. [27] 53.6% (30/56) 29.4% (5/17) NR

Completion rate %
Neubrand et al. [44]a 65.6 45.3 NR NR
Widdice et al. [45]b 32.5 26.3 14.9 NR

Completion rate % Eligible girls vaccinated

Dempsey et al. [20] dose 2a 81 67 70 NR
dose 3a 78 63 30 NR
a
p < 0.0001.
b
p < 0.001.
c
Adjusted for race, age, medical specialty and visit type.
d
Adjusted for race/ethnicity, age, household income and parent education.
e
Adjusted for practice location, parent’s age, adolescent’s age, urbanicity, insurance, race/ethnicity, perception of vaccine safety.
f
Adjusted for insurance, DMPA vaccination and months since vaccine available.

the vaccination program. Four studies report that African Ameri-
can girls were least likely to complete the program [19,20,28,45].
(Table 4) One study reported that Hispanic girls were least likely
to receive all three vaccines (61.2% did not complete the program).
However, a large study (Chao et al.) found that Hispanic girls were
more likely than Black girls, but less likely than Caucasian girls to
get all three vaccine doses. One study reported no significant dif-
ference in completion between Hispanic girls and Caucasian girls
[19] (Table 3).
3.4.2. Girls’ age
Age was reported in six studies as a possible predictor for series
completion [17–20,44,45]. Two studies [20,44] reported no sig-
nificant difference in age group. Two studies report that older
adolescents were more likely to complete the program [17,45].
However, two other studies [18,19] reported that 16–18-year-old
girls were less likely to complete the program (Table 4).
3.4.3. Healthcare coverage
Having health insurance (either private or public) was asso-
ciated with higher completion rates in three studies (p < 0.001)
[20,44,45], although series completion was highest in the private
health insurance group, compared to the public health insurance
group (p < 0.0001) [44]. In another study, longer enrolment in the
U.S. Medicaid program predicted vaccine completion [19] (Table 5).
3.4.4. Other factors
Two studies reported no significant correlation between receiv-
ing three doses of the HPV-vaccine and the initiation of sexual
activities [19,44]. Distance from home to the clinic and geographic
region were also not predictive for program completion [19,44]
in these studies. A gynecological exam and/or Pap test within 3
years prior to initiating the vaccine [44], the receipt of other ado-
lescent vaccines with the HPV-dose [20] and poverty status [17]
were reported as non-significant. Chao et al. [18] reported that a
higher neighborhood education level, a higher number of histori-
cal primary care provider visits and a history of allergy to antibiotic
use (independent of the number of primary care provider visits)
were positively associated with regimen completion.
4. Discussion
To our knowledge this is the first systematic review of factors
influencing actual HPV vaccine uptake, since previous system-
atic reviews have primarily focused on vaccine acceptability and
intention to vaccinate, not actual uptake [11,12,46]. This review
confirms the findings of these previous reviews identifying a range
of important predictors to vaccination including: the vaccinated
girl’s race or ethnicity, age, health insurance status, previous vac-
cination history, and knowledge about HPV, cervical cancer and
the HPV vaccine. Parental vaccine knowledge was also important.
These findings are also similar to studies of the uptake of other ado-
lescent vaccines such as Hepatitis B and to some extent influenza
[47–51]. Table 6 summarizes the study findings.
For both HPV vaccine initiation and completion there was a clear
indication that having an ethnic background of Caucasian was asso-
ciated with higher rates of vaccination. However, it is unclear to
what extent ethnicity/race may apply in healthcare settings out-
side of the United States, or whether ethnicity/race may be acting
as a proxy for socioeconomic status. There are substantial racial
and ethnic disparities in terms of burden of HPV infection and cer-
vical cancer incidence in the United States with African American,
Hispanic and Asian/Pacific Islander women experiencing a higher
burden of disease compared to Caucasian women [52–54]. Simi-
larly, in the United States, girls without health insurance were less
likely to initiate or complete the vaccination program. Cervical can-
cer and HPV incidence rates are much higher among women living
in poorer and less educated counties than among women living
in wealthier areas [52,53]. Given the higher burden of disease and
increased risk in these disadvantaged populations, specifically tar-
geted vaccination programs and innovative methods to increase
accessibility and improve uptake rates are required.
Place of vaccination (school-based vs. doctor’s office or other
location) was not included as a predictive factor in any included
Table 6
Summary—predictors of HPV vaccine uptake in teenage girls.

Author Study N Risk of Predictors of vaccine initiation and completion Factors controlled in multivariate analysis
bias
Race/ Age Vaccine Area of Parental Family Health Healthcare Beliefs, Knowledge Information Physician Race/ Girls Healthcare Family Parental
ethnicity History residence education income care coverage attitudes recomm. ethnicity age coverage income education
utilization and
intentions
Initiation
√ √ √ √ √ √
Brewer et al. [24] 650 L × × × • •
√ √ √ √
Chao et al. [18,28,43] 285,265 L • • • • •
√ √ √ √
Cook et al. [19] 167,082 L • • •
√ √ √ √ √
Dempsey et al. [20] 10,082 L • • •
√ √ √
•

S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556

Ogilvie et al. [22] 2025 L
√ √ √ √
Reiter et al. [32] 617 L × × × • •
√ √ √
Pruitt and 1709 L–M × × • • • • •
Schootman [31]
√
Agius et al. [21] 2926 M
√ √ √
Allen et al. [30] 476 M × ×
√ √ √ √
Caskey et al. [37] 412 M × × ×
√
Cates et al. [40] 696 M • •
√ √
CDC [17] 9621 M ×
√
McCave [33] 227 M
√ √
Rand et al. [29] 430 M × × ×
√ √ √
Roberts et al. 2817 M ×
[23,41,42,69]
√ √ √ √
Rondy et al. [36] 384,869 M
Rosenthal et al. [38] 153 M × •
√
Rouzier and 77,744 M
Giordanella [34]
√ √
Staras et al. [35] 237,015 M ×
√ √
Mathur et al. [39] 155 M–H
√
Dempsey et al. [25] 52 H
√ √ √ √ √
Gerend et al. [26] 82 H ×
√ √
Yeganeh et al. [27] 95 H × × ×

Completion
√ √ √ √
Chao et al. [18,28,43] 285,265 L • • • • •
√ √ √
Chao et al. [28] 167,082 L × • • •
√ √
Dempsey et al. [20] 10,082 L × × • • •
√ √
CDC [17] 9621 M ×
√ √
Neubrand et al. [44] 352 M × × ×
√ √ √
Widdice et al. [45] 3297 M
This table summarizes the study findings, together with risk of bias assessed for each study (L – low, M – moderate, H – high), and an indication of whether important confounding factors were controlled for in multivariate analysis. Predictors
√
of vaccine initiation and completion are shown in the table by the following symbols: – significant association detected; × – no significant association detected; • – indicate factors were included in multivariate analysis.

3553
3554 S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556
study. However, we note that in the included studies the uptake rate
in studies with a school-based program was considerably higher
(range 65–86%) [22–24,45–47], than in studies which did not have a
school-based program (range 19–71%). This is consistent with Skin-
ner and Cooper Robbins [9] who reported that the most acceptable
way to achieve high uptake of HPV vaccine is to offer voluntary
school-based vaccination. It is not known if school based vacci-
nation programs have the ability to also narrow the disparities
between racial and ethnic groups, as only one study reported racial
differences in a school based program [23].
There are some indications that commencing the HPV vaccina-
tion series at a younger age (12 years or younger) is preferable
as there may be increased vaccine effectiveness if the vaccine is
received prior to the commencement of sexual activity [1,55,56].
However we found some evidence that, to date, older adolescents
(between 15 and 18) are more likely to have initiated or com-
pleted the HPV vaccination course than younger adolescents. Many
national HPV vaccination programs specifically target younger girls
(aged around 12), and most countries had time limited vaccina-
tion for older girls. However, catch-up and other programs which
specifically targetted older adolescents when the HPV vaccine was
introduced may have been effective in increasing uptake in this
age group initially, with subsequent messaging regarding the effec-
tiveness of the vaccine prior to sexual debut influencing uptake in
younger girls thereafter. In Australia, the national HPV vaccination
registry (which collects data all vaccinations provided free to girls
and women aged between 11 and 26) has shown that vaccination
rates are higher for younger teenage girls than for older teenage
girls (completion rate for girls aged 11–12, 73% compared with
66% for 16–17-year-old girls). Completion rates for older teenage
girls and women in community/GP settings are much lower again
(17–19 38%, 20–26 30%), reflecting both the effect of increasing
age, but also the higher uptake associated with school-based vac-
cination programs [57,58]. It may also be the case that in the
absence of school-based programs targeting younger adolescents,
older teenage girls and their parents become more aware of the
need for HPV vaccination and seek it out. The variability in vaccine
uptake across countries suggests that there is a complex interplay
of systemic and individual factors influencing uptake and it will be
important to monitor vaccine initiation and completion rates into
the future to ensure that programs can identify whether a more
targeted approach based on age is indicated.
Monitoring both initiation rates and completion rates for HPV
vaccination and identifying factors associated with both may also
be important since little is known about the consequences of
delayed doses or incomplete vaccination on the efficacy of the
HPV-vaccine. It is possible that adolescents currently enrolled in
national vaccination programs may have lower immune responses
than reported in clinical trials, where participants are vaccinated
exactly according to the schedule [45]. This may be a problem
because a longer interval between doses 1 and 2 has been found
to be associated with a decreased antibody response in a similar
vaccine, Hepatitis B, whereas delays between the second and third
dose are unlikely to affect immunogenicity [59].
Vaccination history also seems to be predictive for HPV vaccine
initiation. We found that girls who had previously received the
meningococcal vaccine or the MMR-vaccine were more likely to
initiate the HPV vaccination program. We also found that parental
beliefs and attitudes about vaccination did influence initiation and
completion rates, in particular perceived vaccine safety and the per-
ceived possibility of the vaccine causing side effects. These factors
are also reported in studies about anticipated vaccine acceptance
[13]. Related to parental beliefs and attitudes about vaccination is
knowledge about HPV infection and HPV vaccination, both among
parents and among adolescent girls themselves. We found that girls
who had a higher knowledge about HPV and the vaccine were more
likely to be vaccinated, and caregivers of vaccinated children had
a significantly higher HPV-vaccine related knowledge than care-
givers of non-vaccinated children. This corresponds with previous
studies which showed increased vaccine-related knowledge asso-
ciated with HPV-vaccine acceptance and intention to vaccinate
[60–62]. However, as the studies were cross sectional it is impos-
sible to determine whether the relationship is consequential or
predictive.
The primary care provider seems to play an important role in
providing HPV-related information and assisting girls to initiate
and/or complete the vaccine series (at least in settings where a
school-based program is not offered). Girls that visited their health-
care provider in the past twelve or six months had a higher vaccine
uptake, and no preventive care visit in the past year was associ-
ated with vaccine refusal. Since parental decision making is largely
influenced by the quality and the source of information, it is impor-
tant to provide correct information by a reliable source, e.g. schools
or a primary care provider. This could have a significant impact
on beliefs, attitudes and intentions regarding HPV-vaccination of
parents with an adolescent daughter.
4.1. Limitations of the review
Many of the included studies had substantial limitations with
respect to the generalizability of the results outside of the US
health care setting, the validity of outcome measures and study
designs. We were not able to statistically pool any of the results
of these surveys due to heterogeneity of study populations and
there was no consistency in which adjustment variables were
included across studies. Furthermore, the vaccination uptake rates
in the included studies were all relatively low, which may have
reflected the relative infancy of the vaccination programs at the
time that the studies were conducted. As a result of the limitations
of the data we found considerable variability in study findings and
inconsistency in the direction and magnitude of effect for some of
the important factors identified, leading to the conclusion that con-
siderable uncertainty remains about which are the most important
factors influencing HPV vaccine initiation and completion. The
large number of US-based studies and systemic differences in the
provision of HPV vaccination between the US and other developed
countries and between developed and developing countries may
significantly limit the applicability of particular findings outside
the US healthcare setting. Generalizability may also have been
limited by our decision to exclude studies not published in English,
and this body of evidence may not provide guidance about the
factors influencing uptake of HPV in developing countries, or in
parts of Latin America and Asia. Despite these limitations we were
able to draw a number of important conclusions.
5. Conclusions
The aims of this systematic review were to evaluate factors
associated with the success of HPV vaccination programs for
(pre-)adolescent girls in increasing vaccine coverage in this
population. Important factors influencing initiation and
completion of the HPV vaccination series included race/ethnicity,
girls’ age, parental and adolescent knowledge about HPV and
vaccination and healthcare utilization. However, the quality of the
included studies limits the conclusions we can make about the rela-
tive importance of different factors or the size of their effects. There
were less data about completion of the 3 dose series than about
initiation and, as national vaccination programs mature, further
research about the importance of a complete vaccine series and the
factors which influence completion are required. The possibility
that racial disparities could be, at least partially, addressed by a
universal school-based immunization program should be explored.
 S.J.M. Kessels et al. / Vaccine 30 (2012) 3546–3556
Acknowledgments
Annette Braunack-Mayer, Helen Marshall and Maureen Wat-
son are investigators on an Australian Research Council Linkage
Grant Project (LP100200007) known as Health Bridges, which is
investigating intersectoral collaboration and the school-based HPV
immunization program, and Rebecca Tooher is the project manager
on this grant. We would like to acknowledge the helpful comments
provided by the other Health Bridges investigators: Maree O’Keefe,
Rachel Skinner, Kirsten McKaffrey, Teresa Burgess, and Heather
Ashmeade.
Contributors: All authors made substantial contributions to the
conception and design of the study, and to revising it for critically
important intellectual content. SK and RT were also responsible for
acquisition and analysis of data and drafting the article. All authors
have seen and approved the final version submitted.
Appendix A. Supplementary data
Supplementary data associated with this article can be found, in
the online version, at doi:10.1016/j.vaccine.2012.03.063.
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