Knowledge, Attitudes and Awareness of The Human Papillomavirus Among Health Professionals in New Zealand
Knowledge, Attitudes and Awareness of The Human Papillomavirus Among Health Professionals in New Zealand
Knowledge, Attitudes and Awareness of The Human Papillomavirus Among Health Professionals in New Zealand
Background
OPEN ACCESS
Human papillomavirus (HPV) is a common sexually transmitted infection that is implicated
Citation: Sherman SM, Bartholomew K, Denison
in 99.7% of cervical cancers and several other cancers that affect both men and women.
HJ, Patel H, Moss EL, Douwes J, et al. (2018)
Knowledge, attitudes and awareness of the human Despite the role that HPV plays in an estimated 5% of all cancers and the evolving role of
papillomavirus among health professionals in New HPV vaccination and testing in protecting the public against these cancers, preliminary
Zealand. PLoS ONE 13(12): e0197648. https://doi. research in New Zealand health professionals suggest knowledge about HPV may not be
org/10.1371/journal.pone.0197648
sufficient.
Editor: Ray Borrow, Public Health England,
UNITED KINGDOM
Methods
Received: May 3, 2018
A total of 230 practice nurses, smear takers and other clinical and laboratory staff who
Accepted: December 10, 2018
attended a range of training events completed a cross-sectional survey between April 2016
Published: December 31, 2018 and July 2017. The survey explored four broad areas: demographics and level of experi-
Copyright: © 2018 Sherman et al. This is an open ence, HPV knowledge (general HPV knowledge, HPV triage and test of cure (TOC) knowl-
access article distributed under the terms of the edge and HPV vaccine knowledge), attitudes towards the HPV vaccine and self-perceived
Creative Commons Attribution License, which
adequacy of HPV knowledge.
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited. Results
Data Availability Statement: The information The mean score on the general HPV knowledge questions was 13.2 out of 15, with only
sheet, survey and data are deposited publicly on
25.2% of respondents scoring 100%. In response to an additional question, 12.7% thought
the Open Science Framework website and can be
accessed here: osf.io/ub7g2, DOI 10.17605/OSF. (or were unsure) that HPV causes HIV/AIDS. The mean score on the HPV Triage and TOC
IO/UB7G2. knowledge questions was 7.4 out of 10, with only 9.1% scoring 100%. The mean score on
Funding: The authors received no specific funding the HPV vaccine knowledge questions was 6.0 out of 7 and 44.3% scored 100%. Only
for this work. 63.7% of respondents agreed or strongly agreed that they were adequately informed about
Competing interests: The authors have declared HPV, although 73.3% agreed or strongly agreed that they could confidently answer HPV-
that no competing interests exist. related questions asked by patients. Multivariate analyses revealed that knowledge in each
Discussion
Although overall level of knowledge was adequate, there were significant gaps in knowl-
edge, particularly about the role of HPV testing in the New Zealand National Cervical
Screening Programme. More education is required to ensure that misinformation and stigma
do not inadvertently result from interactions between health professionals and the public.
Introduction
Human papillomavirus (HPV) is responsible for 99.7% of cases of cervical cancer along with
some head and neck, penile and anal cancers. There are approximately 150 new diagnoses and
50 deaths from cervical cancer in New Zealand (NZ) every year [1], while head and neck can-
cers attributable to HPV are increasing in both men and women with 94 new cases and 43
deaths estimated for 2012 [2]. In addition, there are longstanding ethnic inequalities in cervical
cancer incidence and mortality, and cervical screening coverage remains low (and cancer inci-
dence and mortality high) for indigenous Māori women as well as Pacific women [3].
The NZ National Cervical Screening Programme (NCSP), which was established in 19904,
recommends 3-yearly routine screening with liquid-based cytology (LBC) for 20–69 year-old
women, with HPV triage testing for low grade (ASC-US/LSIL) cytology in women 30+ years.
The programme also recommends testing of cure following treatment for a high-grade lesion
[4]. From late 2018 the NCSP will introduce HPV testing as the primary screening test for
women aged 25–68 years on a 5 yearly basis [5].
To reduce infection with high-risk types of HPV and its related cancers, the NZ National
HPV Immunisation Programme was introduced in September 2008, offering free HPV vacci-
nation (Gardasil, Merck) for females born in 1990 or later. School-based immunisation for
12–13 year-old girls commenced in most regions in 2009 [1] and the three-dose coverage
achieved by the program in cohorts born in 1991–2002 reached approximately 48–66% nation-
wide [1]. In January 2017, the free programme was extended to boys and young men, the
upper age for free vaccination was increased to 26 years, a two-dose schedule was implemented
for individuals aged 14 and under, and the vaccine used was changed to nonavalent Gardasil 9
(Merck) [1].
Previous research has identified that health professionals can play an important role in vac-
cine uptake. In an Italian survey assessing childhood vaccine hesitancy in parents, hesitancy
was significantly more common in those parents who lacked confidence in their child’s doctor
[6]. In a US study, more adolescents had not had the HPV vaccine when their parents felt they
were not able to openly discuss their concerns with the doctor [7] and in a second US study of
parents who decline then later accept the HPV vaccination for their child, secondary accep-
tance was more likely in parents who received follow-up counselling from their child’s health-
care provider [8]. Furthermore, recent research in the UK has also identified that women who
report greater trust in their doctor were less likely to have decided not to undergo cervical
screening [9].
In NZ, a cervical sample taker is a registered health practitioner (nurse or doctor) who
holds a current practising certificate and has completed appropriate cervical screening train-
ing as part of a medical degree, midwifery training programme or via a New Zealand
Qualifications Authority (NZQA) accredited course for cervical sample takers. Previous
research exploring the knowledge of GPs and practice nurses (PNs) in Christchurch, New
Zealand about HPV used 5 questions as part of a larger survey exploring attitudes towards
HPV vaccination [10]. Whilst performance across the 5 questions was reasonable, there was
uncertainty as indicated by the number of ‘not sure’ responses, as well as some variability
across questions. For example, while more than 90% of GPs and PNs knew that HPV vaccina-
tion would not eliminate the need for cervical screening, only 33% of GPs and 7% of PNs
knew that anogenital warts caused by HPV 6 and 11 are not a precursor to cervical cancer.
Only half of GPs and 42% of PNs knew that most HPV infections will clear without medical
treatment and a quarter of GPs and nearly a third of PNs did not know, or were unsure,
whether persistent HPV was a necessary cause of cervical cancer.
To our knowledge there are no studies exploring what primary care staff such as GPs, PNs
and smear takers in NZ know about HPV since 2009. In light of the recent changes to the
immunisation programme and the forthcoming changes to the NCSP, it is important to
benchmark what nurses and smear takers understand about HPV, whether they feel well
informed and assess any training needs they might identify.
Methods
Ethics approval was granted by the Massey University Ethics Committee 4000015595. The
project was registered with Waitemata DHB localities (Reference number RM13518). Both
Waitemata and Auckland DHB confirmed that locality authorisation was not required as the
research was carried out in community healthcare settings.
An anonymous cross-sectional survey was conducted between April 2016 and July 2017.
GPs, practice nurses, smear takers and other clinical and laboratory staff who attended a vari-
ety of training events (11 in total) in Auckland District Health Board (DHB), Hutt Valley DHB
and Waitemata DHB catchment areas were invited to complete the paper-based survey. The
sample represents the number of respondents we were able to collect within the one-year time
frame. Participants were provided with an information sheet to read prior to completing the
survey. The survey was taken from Patel et al., [11] who had incorporated most of the items
from Waller et al., [12] and was adapted by adding back in a question about HPV and HIV/
AIDS from Waller et al., and by changing some wording to make the terminology or protocols
New Zealand-specific.
We established the face validity of the adapted questionnaire for the NZ clinical environ-
ment by having two groups peer review the survey, firstly to ensure we had captured the scope
adequately and secondly to ensure questions were well structured. These groups included
members of the DHB Immunisation team and cervical screening specialist doctors as well as
nurse practitioners.
The final survey explored four broad categories: demographics and level of experience;
HPV knowledge (general HPV knowledge, HPV triage and test of cure (TOC) knowledge and
HPV vaccine knowledge), which were assessed using a true, false, don’t know format; and atti-
tudes towards the HPV vaccine and self-perceived adequacy of HPV knowledge, which were
assessed using 5-point Likert scales (the survey is publicly available here: osf.io/ub7g2, DOI 10.
17605/OSF.IO/UB7G2).
Statistical analyses
Demographic factors included age, profession and years since HPV training. For analyses, pro-
fession was collapsed into four categories (nurse; general practitioner (GP); colposcopy, which
included colposcopists and colposcopy nurses; and laboratory staff and other), and years since
HPV training was collapsed into 3 categories (never; � 1 year; > 1 year).
Factors affecting HPV knowledge were assessed using ordinal regression analysis. The
approach for model development was to conduct univariate analyses initially and then enter
variables into the full multivariate models that showed a statistically significant (P<0.05) asso-
ciation with the main outcomes in the univariate analyses. The rationale for this was that if a
variable was associated with the main outcome measure, it could be a confounder.
Factors affecting self-perceived adequacy of HPV knowledge were also assessed. Feeling
adequately informed and feeling confident in answering patient questions were converted
from 5-point Likert scales to binary variables of yes (strongly agree, agree) and no or unde-
cided (strongly disagree, disagree or undecided) as the dependent variables.
Results
A total of 234 health professionals completed the survey. Due to the opportunistic nature of
participant recruitment, a response rate was not able to be calculated. The data for four indi-
viduals were removed, as there were large sections that had been left unanswered. A total of 22
health professionals had at least one answer missing for the general HPV knowledge questions,
18 had at least one answer missing for the Triage and TOC knowledge questions, and 8 health
professionals had at least one answer missing for the vaccine knowledge questions. Overall, 40
participants had at least one answer missing across all of the questions (several participants
had missing data in more than one of the three sections). Details about participant gender, age
categories, profession, smear taker status and date of most recent training, if any, are presented
in Table 1.
https://doi.org/10.1371/journal.pone.0197648.t001
still require annual follow up for life (39.1%); If cytology and high-risk HPV test are negative
at 12 and 24 post treatment, they will require a repeat smear in 3 Years (24.4%). In addition,
more than 10% of health professionals incorrectly thought (or weren’t sure) that an HPV test
can tell how long a person has had an HPV infection; an HPV test cannot be done at the same
time as a Smear test; HPV testing is used to indicate if the HPV vaccine is needed; when an
HPV test has been done that the results are available the same day; If an HPV test shows that a
women does not have HPV her risk of cervical cancer is not low.
https://doi.org/10.1371/journal.pone.0197648.t002
The following questions were answered incorrectly most often: The HPV vaccine offers
protection against genital warts (31.9% answered incorrectly or weren’t sure); The HPV
vaccines offer protection against most cervical cancers (18.8%); The HPV vaccines are most
effective if given to people who have never had sex (17.5%). In addition, more than 10% of par-
ticipants incorrectly thought (or weren’t sure) that the recommended number of HPV vaccine
doses was not three.
https://doi.org/10.1371/journal.pone.0197648.t004
In total, 94.3% (N = 215) respondents agreed or strongly agreed that men/boys should be
offered the vaccine (Table 4), with 5.3% (N = 12) undecided and 0.4% (N = 1) in disagreement
(there were 2 blank responses).
Table 5. Logistic regression of the effect of knowledge on feeling adequately informed / confident in answering patient questions.
Feeling adequately informed
Crude Adjusted for ever taken a smear, years since training and
current role
OR 95% CI p OR 95% CI p
HPV knowledge 1.34 1.11–1.61 <0.01 1.14 0.93–1.39 0.22
Triage and TOC knowledge 1.30 1.12–1.52 <0.01 1.07 0.89–1.29 0.48
HPV vaccine knowledge 1.66 1.29–2.14 <0.01 1.65 1.21–2.24 <0.01
Feeling confident in answering patient questions
Crude Adjusted for ever taken a smear, years since training and
current role
OR 95% CI p OR 95% CI p
HPV knowledge 1.48 1.22–1.79 <0.01 1.22 0.98–1.52 0.08
Triage and TOC knowledge 1.62 1.36–1.94 <0.01 1.24 1.00–1.53 0.05
HPV vaccine knowledge 2.10 1.60–2.78 <0.01 2.16 1.47–3.17 <0.01
https://doi.org/10.1371/journal.pone.0197648.t005
Feeling adequately informed and confident in answering patient questions were indepen-
dently predicted by HPV vaccine knowledge after adjustment for the other predictors, while
the associations with HPV knowledge and Triage and TOC knowledge disappeared after
adjustment. Again, the number of health professionals in the colposcopy role category was
very small, so these results should be interpreted with caution.
Improving training
Suggestions for how training might be improved were provided by 36 respondents (15.7%).
They wanted regular updates, more training sessions and several health professionals felt that
online training and other online resources such as research, frequently asked questions and
updates would be useful. A request for specific advice that should be provided to parents and
simple information sheets for both primary care and patients was suggested. There were also
requests to widen the provision of training beyond practice nurses to all healthcare providers,
specifically including GPs, independent vaccinators and Public Health Nurses delivering the
School Based Immunisation programme.
Discussion
Although mean knowledge levels for HPV and the HPV vaccine were reasonable (with each
subset of questions yielding a mean percentage correct score of between 88% and 85%, respec-
tively), only 25.2% and 44.3% of health professionals scored 100% in each category, respec-
tively. Research has been conducted in other countries with HPV vaccination programmes to
explore health professional knowledge about HPV and the vaccination (e.g., [11, 13, 14]).
These studies reveal that, consistent with our NZ results, health professional knowledge about
HPV and the HPV vaccination is frequently incomplete.
An evaluation of knowledge about HPV and HPV vaccination for GP practice nurses in
Leicestershire in the UK, where the vaccination has been administered through the NHS since
2008, found that although general HPV knowledge scores were quite high, there were specific
gaps or weaknesses in knowledge [11] for example nearly 10% of PNs did not know that HPV
causes cervical cancer and 63% believed that HPV requires treatment. Our study also revealed
significant gaps in knowledge. For example, while general HPV knowledge was high, around a
quarter of respondents were unaware that having sex at an early age increases the risk of get-
ting HPV. A quarter of respondents were also unaware that HPV is so common that most sex-
ually active people will be exposed to it in their lifetime. Research has shown that considerable
stigma can be attached to a positive HPV test [15, 16] and that a lower level of education can
be associated with an increase in the negative emotions and stigma that patients experience
[16]. Therefore, it is vital that clinical staff are aware of the widespread nature of the virus so
that they can reassure patients and reduce stigma. A third of participants did not know or were
unclear that HPV does not usually need treatment. This lack of knowledge has the potential to
spread misinformation and cause confusion among patients as they seek treatment that is not
available. Perhaps most worryingly, 13% of respondents either believed that HPV causes HIV/
AIDS or were unclear that it did not.
Other research has demonstrated a lack of complete knowledge about HPV and the HPV
vaccine among health professionals. Nilsen et al explored knowledge of and attitudes to HPV
infection and vaccination among public health nurses and GPS in Northern Norway in 2010,
one year after the HPV vaccination was introduced for 12 year-old girls in Norway [13].
Knowledge of HPV infection, vaccine and cervical cancer was measured with 7 open-ended
questions (e.g. what is the lifetime risk of a sexually active person getting HPV?). The percent-
age of GPs getting each question correct ranged from 26–55% while for the nurses it was 35–
86%. Self-reported knowledge was considerably higher than actual knowledge. Only 47% of
respondents knew that HPV infection is a necessary cause of cervical cancer.
In Malaysia there has been a school-based HPV vaccination programme since 2010. Jeya-
chelvi et al conducted a survey to explore HPV and HPV vaccination knowledge and attitudes
in primary health clinic nurses who run the vaccination program in Kelantan, Malaysia [14].
Nurses were given 11 questions to assess their knowledge. The mean score was 5.37 with the
minimum score being 0 and the maximum being 9. No question was answered correctly by
more than 87.3% of respondents and the poorest question (External anogenital warts increase
the risk of cancer at the same site where the warts are located. True/False) was answered cor-
rectly by only 10.6%.
Rutten et al conducted a survey exploring clinician knowledge, clinician barriers and per-
ceived parental barriers to HPV vaccination in Rochester US [17]. They found that greater
knowledge of HPV and the HPV vaccination (assessed together using an 11-item scale) was
associated with higher rates of HPV vaccination initiation and completion of the 3-dose vacci-
nation schedule, suggesting that knowledge is important in order to effectively promote HPV
vaccination in addition to reducing stigmatising attitudes of clinicians identified in past
research [18] and discussed in more detail below.
Knowledge about triage and test of cure in our study was lower than for HPV and HPV vac-
cine knowledge (mean percentage correct score of 74%) and only 9.1% of health professionals
correctly answered all the answers in this section. The Leicester UK study discussed above also
revealed gaps in the practice nurse knowledge about current NHS processes around HPV tri-
age and test of cure [11]. For example, the role of HPV testing post-treatment (TOC) was mis-
interpreted, with only 66% acknowledging that all normal, borderline nuclear and mildly
dyskaryotic samples are tested for high risk HPV post-treatment. Not all nurses felt adequately
informed about HPV and a need to improve the provision of training was identified. For the
triage and test of cure questions, while some questions were generally answered accurately in
our study, some questions revealed uncertainty and a lack of understanding of the current
guidelines. For example, fewer than half of the respondents knew that not all cervical samples
showing mild cellular changes are tested for high-risk HPV (only those for women aged 30
and older are tested for HPV under the current NZ guidelines). In addition, almost a quarter
of respondents did not know or were unsure that a negative HPV test means that a woman is
at low risk from cervical cancer. This uncertainty is likely to be problematic when primary
HPV testing is rolled out. Unlike the cell changes that are screened for currently, primary HPV
screening is about identifying a woman’s risk factors. Health professionals will need to be con-
fident in talking with women about what their positive test result means. The test of cure ques-
tions were also correctly answered by fewer than three quarters of the respondents.
In addition to knowledge, other studies have been conducted exploring health profession-
als’ attitudes towards the HPV vaccine. In Italy, almost all of the primary care paediatricians
surveyed believed the vaccine was effective in preventing HPV related diseases in boys (92.3%)
and girls (97.9%) and they also believed it was safe. Despite this only 18.4% always recom-
mended the HPV vaccine to boys aged 11–12 compared with 77.4% who always recommended
it to girls aged 11–12 [19]. In a French survey, 72.4% of general practitioners indicated that
they always or often recommended the vaccine to girls aged 11–14 [20], while in a US survey,
60% of paediatricians and 59% of family doctors recommended the vaccine to girls aged 11–12
compared with 52% and 41% who recommended it to boys aged 11–12 [21]. By contrast in
our survey, the vast majority of health professionals indicated that they would recommend the
vaccine and they also favoured vaccinating boys and men, with only one individual indicating
they would not recommend vaccinating boys and men. This is particularly reassuring since
NZ made the vaccine available to boys from January 2017.
The need for education indicated by the knowledge scores was further reinforced by the
fact that over a third of respondents did not agree that they felt adequately informed about
HPV and that being adequately informed and feeling confident in responding to patients’
questions were both associated with knowledge. Suggestions for training were proposed by
some of the respondents. One promising suggestion, which was also proposed by UK practice
nurses [11], was for online training. This would provide a low-cost way to update changes to
the vaccination and/or screening programmes and guidelines in a format that would be easily
accessible to many staff whilst requiring relatively little time commitment to complete. HPV
vaccination online training was developed by the Immunisation Advisory Committee (IMAC)
and was released in August 2017 [32]. This may address some of the knowledge issues associ-
ated with vaccination identified in this study, but additional online training regarding screen-
ing and test of cure is needed.
Limitations
There are several limitations to our study. Firstly, due to the opportunistic recruitment
approach, involving self-selection of study participants, the response rate is unknown. As a
consequence, we were not able to examine whether, and to what extent, bias due to non-
response (or participation bias) has occurred, as we were unable to assess the level of HPV
knowledge in non-responders. Also, as is common for most questionnaire surveys, we cannot
exclude social desirability bias (the tendency of survey respondents to answer questions in a
manner that will be viewed favourably by others), but believe that this type of bias is less likely
to be a significant factor for health professionals. Secondly, the sample is not evenly distrib-
uted across the categories of health professionals, with significantly more nurses having com-
pleted the survey than GPs, colposcopists or laboratory and other staff. Since there are
currently no official data available on the cervical screening workforce in New Zealand, we
are unable to indicate how representative our sample is of that wider group. Thirdly, some of
the questions, such as whether participants felt they could confidently answer HPV related
questions asked by patients, are less relevant to laboratory staff who are less likely to interact
with patients. Lastly, as with all such surveys, by providing questions with true/false/don’t
know response options, the questions themselves might act as a prompt enabling educated
guesses rather than measuring knowledge directly and thus might potentially overestimate
knowledge.
Concluding comments
Our survey is the first to be conducted in NZ that explores health professional knowledge and
understanding about HPV, the vaccine and the role of HPV testing in the cervical screening
programme and it contributes to the international picture about HPV knowledge that is
emerging. It is evident from our findings and those from other countries, that more education
is required to ensure that misinformation, the stigma associated with the sexually transmitted
nature of HPV and widening inequalities do not inadvertently result from interactions
between health professionals and the public.
Acknowledgments
We would like to thank the following individuals for assistance with data collection:
Jane Grant—Cervical Screening Nurse Specialist, Metro Auckland Cervical Screening
Coordination Service, Auckland and Waitemata DHBs
Lucina Kaukau—Cervical Screening Nurse Specialist, HPV Self-Sampling Feasibility study
for Maori women, Research Nurse.
Author Contributions
Conceptualization: Susan M. Sherman, Karen Bartholomew, Hayley J. Denison, Collette
Bromhead.
Data curation: Karen Bartholomew, Hayley J. Denison, Collette Bromhead.
Formal analysis: Susan M. Sherman, Hayley J. Denison, Jeroen Douwes.
Methodology: Susan M. Sherman, Collette Bromhead.
Project administration: Collette Bromhead.
Resources: Karen Bartholomew, Collette Bromhead.
Validation: Karen Bartholomew.
Writing – original draft: Susan M. Sherman.
Writing – review & editing: Susan M. Sherman, Karen Bartholomew, Hayley J. Denison, Her-
sha Patel, Esther L. Moss, Jeroen Douwes, Collette Bromhead.
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