Acceptability and Correlates of Primary and Secondary Prevention of Cervical Cancer among Medical Students in Southwest China: Implications for Cancer Education
et al. (2014) Acceptability and Correlates of Primary and Secondary Prevention of Cervical Cancer among
Medical Students in Southwest China: Implications for Cancer Education. PLoS ONE 9(10): e110353. doi:10.1371/journal.pone.0110353
Acceptability and Correlates of Primary and Secondary Prevention of Cervical Cancer among Medical Students in Southwest China: Implications for Cancer Education
Xiong-Fei Pan 0
Zhi-Mei Zhao 0
Jing Sun 0
Feng Chen 0
Qing-Lian Wen 0
Kang Liu 0
Gui-Qin Song 0
Jing-Jing Zhang 0
Ying Wen 0
Chun-Jing Fu 0
Chun-Xia Yang 0
Yue Wang, National Institute for Viral Disease Control and Prevention, CDC, China, China
0 1 Department of Epidemiology, West China School of Public Health, Sichuan University , Chengdu , China , 2 Department of Pathology, Development and Regeneration Key Laboratory of Sichuan Province, Chengdu Medical College , Chengdu , China , 3 Department of Preventive Healthcare and Hospital Infection Control, Deyang People's Hospital , Deyang , China , 4 Department of Oncology, the Affiliated Hospital of Luzhou Medical College , Luzhou , China , 5 Institute of Tissue Engineering and Stem Cells, The Second Clinical Hospital of North Sichuan Medical College , Nanchong , China , 6 Department of Biology, North Sichuan Medical University , Nanchong , China , 7 School of Public Health, Kunming Medical University , Kunming , China , 8 Department of Health Statistics and Information Management, School of Public Health and Management, Chongqing Medical University , Chongqing , China
Objectives: To understand knowledge about, and acceptability of, cervical cancer screening and HPV vaccines among medical students; and to explore potential factors that influence their acceptability in China. Methods: We conducted a survey among medical students at six universities across southwest China using a 58-item questionnaire regarding knowledge and perceptions of HPV, cervical cancer, and HPV vaccines. Results: We surveyed 1878 medical students with a mean age of 20.8 years (standard deviation: 1.3 years). Of these, 48.8% and 80.1% believed cervical cancer can be prevented by HPV vaccines and screening respectively, while 60.2% and 71.2% would like to receive or recommend HPV vaccines and screening. 35.4% thought HPV vaccines ought to be given to adolescents aged 13-18 years. 32% stated that women should start to undergo screening from the age of 25. 49.2% felt that women should receive screening every year. Concern about side effects (38.3% and 39.8%), and inadequate information (42.4% and 35.0%) were the most cited barriers to receiving or recommending HPV vaccination and cervical cancer screening. Females were more likely to accept HPV vaccines (OR, 1.86; 95% CI: 1.47-2.35) or cervical cancer screening (OR, 3.69; 95% CI: 2.88-4.74). Students with a higher level of related knowledge were much more willing to receive or recommend vaccines (P,0.001) or screening (P,0.001). Students who showed negative or uncertain attitudes towards premarital sex were less likely to accept either HPV vaccines (OR, 0.67; 95% CI: 0.47-0.96), or screening (OR, 0.68; 0.47-0.10). Non-clinical students showed lower acceptability of cervical screening compared to students in clinical medicine (OR, 0.74; 95% CI: 0.56-0.96). Conclusions: The acceptability of HPV vaccines and cervical cancer screening is relatively low among medical students in southwest China. Measures should be taken to improve knowledge about cervical cancer and awareness of HPV vaccines and screening among medical students at university.
Cervical cancer is the third most common malignancy among
women, with an estimated 528,000 new cases and 266,000 deaths
worldwide in 2012 . In China, its age-standardized incidence
and mortality rates of 7.5 and 3.4 per 100,000 women respectively
are lower than corresponding world statistics (14.0 and 6.8 per
100,000). Given the large population of China, absolute estimates
of cases and mortalities still make it one of the top priorities for
cancer prevention and control.
Cervical cancer can be effectively controlled through primary
and secondary prevention such as cervical screening and
prophylactic HPV vaccination. Since the Papanicolaou (Pap)
smear test was introduced for routine screening, a substantial
decline has been witnessed in cervical cancer deaths in developed
countries in the last four decades . It is a general consensus that
the cytology screening for cervical cancer is effective in reducing
the incidence and mortality in developed countries. Visual
inspection with acetic acid (VIA) or Lugols iodine (VILI), and
HPV DNA-based testing are also utilized for screening purposes in
developing , and developed, countries , respectively.
Prophylactic HPV vaccines have become an established and vital
strategy for primary prevention of cervical cancer . Gardasil
quadrivalent HPV 6/11/16/18 vaccine developed by Merck
(Whitehouse Station, New Jersey, United States) and Cervarix
bivalent HPV 16/18 vaccine by GlaxoSmithKline (Brentford,
London, United Kingdom) are widely available in over 100
countries through regional or national immunization programs.
They had been introduced into national immunization programs
in at least 40 countries by the beginning of 2012 . The
effectiveness and safety of these have been established in clinical
trials and post-market surveillance in populations . A
systematic review of HPV vaccine clinical trials shows that efficacy
is 5090% in preventing intraepithelial neoplasm grade 2+ (CIN
2+) associated with HPV 16 and 18 . Post-market experience
also indicates that vaccine-type HPV prevalence in the US and the
UK  and CIN 2+ incidence in Australia  decreased after
the implementation of population-wide HPV vaccination
However, health care providers have lagged behind in their
efforts to improve screening for cervical cancer in China. There
are no national guidelines for cervical cancer screening, though
non-binding recommendations were made by the China
Foundation of Cancer in collaboration with the Ministry of Health in
2009, that proposed cervical screening every 3 years for women
between 25 and 65 years of age in urban areas, and between 35
and 65 years of age in rural areas . There is no routinely
organized national screening in the country. Since 2009 in rural
China, free screening of cervical cancer has been available to a
limited proportion of the target population in the form of
government-sponsored mass screening . An earlier large-scale
free screening initiative based on visual inspection and cytology
has only covered approximately10 million rural women between
35 and 59 years of age between 2009 and 2012 , while hopes
have been expressed that ongoing efforts will be able to screen 50
million women in rural areas aged 3564 years by 2015. Despite
the increase in reported mortalities due to cervical cancer among
young urban women at an annual rate of 4.1% , women in
urban areas are referred to cervical cancer screening only on an
opportunistic basis, or through employment-based physical
examination . In addition to limited coverage, the effectiveness
of the cervical cancer screening program is hampered by the
limited health care infrastructure available for the latest screening
technologies, which also restrict attempts to promote the services
To date, the two prophylactic HPV vaccines available
internationally are still to be approved by the China Food and
Drug Administration, and are not commercially available in
mainland China . Clinical studies are underway among
Chinese women: Gardasil and Cervarix have already been studied
in trials for over four years, while a new HPV 16/18 vaccine by
Xiamen Innovax Biotech (Xiamen, China) began the phase III
clinical stage in 2013 . An earlier systematic review showed
that 69.7% of cervical cancer cases were attributed to HPV 16/18
in China , which is similar to the estimate (about 70%) at the
global scale . Given these estimates, the efficacy of HPV
vaccines in Chinese trials may hopefully not be very much
different from those from international studies . In addition,
estimated HPV 16/18 positive fractions in high-grade squamous
intraepithelial lesion, low-grade squamous intraepithelial lesion,
and normal women were 45.5%, 32.23% and 4.6%, respectively
. HPV vaccines are expected to effectively avert cervical
morbidity and mortality in China if it was routinely used in
With the rapid scale-up of cervical cancer screening and
anticipation of licensure for prophylactic HPV vaccines in China,
it is important to understand acceptability of, and possible barriers
to, screening and vaccination among the population. To date,
previous studies have explored these issues among women, parents
of adolescents, female university students, health care providers,
and health management staff for HPV vaccines , and
among the female part of the general population for cervical
cancer screening [29,30]. However, none of these studies have
directly surveyed current medical students for their knowledge and
perceptions, although this type of study has been conducted in
other countries . Given that these students will be future
health care providers, their attitudes could influence the success of
screening and vaccination programs. To fill the gap in the
research, we systematically conducted a large-scale survey among
medical students to better understand their knowledge, the
acceptability of cervical cancer screening and HPV vaccines,
and explore potential factors that influence acceptability.
Materials and Methods
1. Study design and population
This cross-sectional study was conducted between May and
September 2013 at six universities across southwest China,
including Sichuan University and Chengdu Medical College in
Chengdu, Luzhou Medical University in Luzhou, North Sichuan
Medical College in Nanchong, Chongqing Medical University in
Chongqing, and Kunming Medical University in Kunming. These
universities are the principle institutions of medical education in
three major provinces in southwest China. We planned to use
200400 medical students from different years of study from each
university as sample to ensure diversity. In addition, 56 whole
classes of medical undergraduates were selected from clinical
medicine and other non-clinical major subjects such as nursing,
dentistry, public health, pre-clinical science, and medical
technological science. Clinical medicine and non-clinical majors have
different foci in China: clinical medicine and dentistry involve
more clinical work, while other major subjects may focus on
medical lab science, health management, public health, and other
health related work. Due to financial and logistic constraints, the
classes from each university were surveyed based on convenient
contact points instead of a random sampling process. The study
was approved by the Ethics Committee of Sichuan University
Fourth Hospital/West China School of Public Health.
2. Study procedure
We used a 58-item questionnaire comprised of three sections of
closed- and open-ended questions relating to basic information
concerning participants, knowledge and perceptions of HPV,
cervical cancer, HPV vaccines, cervical cancer screening, and
sexual attitudes and behavior (Figure S1). The provisional
questionnaire was formulated based on earlier ones used for
similar studies in China  and abroad [33,35] for survey
purposes. It was revised according to comments solicited from
colleagues who had administered similar surveys for earlier studies
. It was piloted by ten medical students in the Chinese
Academy of Medical Sciences Cancer Institute, and changes were
made to the questionnaire based on their comments regarding the
appropriateness of contents and language. The pilot survey
procedure was repeated on another ten medical students from
Sichuan University. The questionnaire was finalized after internal
discussions following the two pilot surveys.
Collaborating staff and medical students were trained on
administering the questionnaire, and conducted the survey before
or after class at each university between May and September 2013.
Survey objectives were explained to potential participants before
each survey. The medical students were free to participate, or not,
at their discretion. The informed consent form was bound together
with the questionnaire when it was handed out to them. Since the
survey was anonymous to protect privacy and ensure data
integrity, there was no request for a signature on the consent
form if they agreed on the survey; they could choose to answer the
questionnaire if they consented verbally or just leave it blank if
they did not after reading the consent form. In accordance with
the ethics committee document, no consent, verbal or written, was
requested from parents or guardians of any participants. Our
surveyors were responsive to queries about the questionnaire itself
during the survey.
Completed questionnaires from each university were delivered
to the Data Management Team in the West China School of
Public Health. Data were entered and managed by the team in a
database that had been developed by EpidData v3.1 (EpiData
Association, Odense, Denmark).
3. Statistical analysis
IBM SPSS 19.0 (Armonk, New York, USA) was used to analyze
the data. Demographic information, selected questions regarding
HPV and cervical cancer related knowledge, and perceptions of
cervical cancer and screening were presented as frequencies and
percentages. Perceptions and concerns of primary and secondary
prevention of cervical cancer were compared between males and
females using the Chi-square test. Univariable logistic regression
analysis was conducted to predict factors influencing the
acceptability of cervical cancer and HPV vaccination, and the overall
predictive model was established using multivariable logistic
regression analysis based on factors of statistical significance. All
tests were two-tailed with a significance level of 0.05.
1. Demographic characteristics
A total of 2150 medical students were approached, and 2000
successfully completed the questionnaires. However, another 122
questionnaires were discarded because they contained answers to
only a few questions, or contained inconsistencies in the answers.
Demographic characteristics of the final 1878 medical students are
summarized in Table 1. These students consisted of 595 males
(32.1%) and 1260 females (67.9%). The mean age was 20.8
(standard deviation: 1.3) years. 91.8% were of Han Chinese
ethnicity, and 43.8% majored in clinical medicine. Most were
second-year (36.2%) and third-year (37%) students. 85.1% of the
students did not have clinical internship at the hospital. Regarding
sexual attitude and behavior questions, 51.0% and 15.2%,
respectively held neutral and positive attitude towards premarital
sexual behavior, and 8.3% had previous experience of sexual
2. Knowledge of HPV, cervical cancer, HPV vaccines and
cervical cancer screening
Responses to selected knowledge questions from the
questionnaire are presented in Table 2. 76.5% of the medical students
were aware of HPV, but only 29% knew there is an HPV vaccine
available worldwide. Only 14.4% thought that persistent HPV
infection was the necessary cause of cervical cancer. 47.8%
thought that cervical cancer may be cured, while 48.8% and
80.1% believed that cervical cancer may be prevented by HPV
vaccines or cervical screening. In addition, 72.6% agreed that
women who had already been vaccinated require cervical
screening. In general, higher percentages of women knew the
correct answer to each selected knowledge question (Table 2).
3. Perceptions of HPV vaccination and cervical cancer
Perceptions of HPV vaccination among medical students are
shown in Table 3. 60.2% of the medical students would like to
receive or recommend HPV vaccination (49.3% for males versus
65.3% for females, P,0.001). 60.8% of female students though
HPV vaccines could be given to boys, as compared to 50.0% of
males students (P,0.001). 36.8% of male, and 34.6% of female,
students preferred HPV vaccination for adolescents aged 1318
years, and 63.5% and 66.0% of them thought that the best time
for HPV vaccination would be before becoming sexually active.
Most students stated that the local Center for Disease Prevention
and Control (CDC) is the most appropriate venue for HPV
vaccination, and the least selected venue was school (24.2% versus
22.2%). Over 70% of medical students were willing to pay a price
lower than 500 RMB (82 USD) for either imported or domestic
vaccines. In addition, 45.8% medical students expressed
preference for imported vaccines, while 36.5% would like to make their
choice according to the price.
Perceptions of cervical cancer screening among medical
students are presented in Table 4. 71.2% of the medical students
would like to receive or recommend cervical cancer screening
(53.6% for males versus 79.4% for females, P,0.001). However,
45.2% and 39.6% of males and females were not aware of any
existing screening techniques. 41.9% and 32% stated women
ought to start being screened from 20 or 25 years, and 49.2% and
42.1% were of the opinion women should receive screening every
year or every 24 years. 82.7% medical students thought a price
below 100 RMB (16.5 USD) was reasonable for cervical cancer
screening per occasion.
4. Concerns of HPV vaccination and cervical cancer
The concern about side effects (38.3% and 39.8%), and
inadequate information (42.4% and 35.0%), were the obstacles
most cited against receiving or recommending HPV vaccination
and cervical cancer screening (Table 5). 81.5% of medical students
favored a future HPV vaccination program in China, but about
half of these would request pricing regulation and subsidy for
5. Correlates with acceptability of HPV vaccines and
cervical cancer screening
Associations of acceptability of HPV vaccination and cervical
cancer screening, with other factors, are presented in Table 6. In
this research, the acceptability corresponds to the two questions on
whether students would like to receive or recommend HPV
vaccination or cervical cancer screening in Table 3 and 4. Six out
of nine variables (eight variables in Table 1 and HPV related
knowledge score) analyzed were significantly associated with the
acceptability of either HPV vaccination or cervical cancer
screening in the univariable logistic analysis, and were thus
incorporated into the multivariable logistic modeling. Female
students were more likely to accept HPV vaccines (OR, 1.86; 95%
CI: 1.472.35) or cervical cancer screening (OR, 3.69; 95% CI:
2.884.74). Students who showed negative attitude towards
Age (years) a
Ethnic groups c
Attitude towards premarital sexual behavior d
Previous sexual behavior e
a,b,c,d,eData were missing for 48, 23, 30, 62 and 67 students, respectively.
premarital sex were less like to accept either HPV vaccines (OR,
0.67; 95% CI: 0.470.96) or screening (OR, 0.68; 0.470.10).
Those who scored high on the level of relevant knowledge were
much more willing to receive or recommend vaccination (P,
0.001) or screening (P,0.001). In addition, non-clinical students
showed lower acceptability of cervical screening compared to
students in clinical medicine (OR, 0.74; 95% CI: 0.560.96).
There were no statistically significant differences in acceptability of
HPV vaccination or cervical cancer screening between students at
different year groups (P = 0.218 and 0.091), and between students
with or without clinical internship (P = 0.854 and 0.180).
Moreover, non-clinical students did not express lower degree of
likeliness to accept HPV vaccination (P = 0.376).
To our knowledge, this is the largest multicenter study that has
explored the acceptability of HPV vaccines and cervical cancer
screening among medical students in China. One major finding is
that 60.2% and 71.2% of medical students were willing to accept
or recommend HPV vaccines and cervical cancer screening,
respectively. Female students and students with improved
knowledge were positive predictors for both HPV vaccines and
screening, while a negative attitude towards premarital sex was a
negative correlate for both. In addition, non-clinical students were
less likely to accept cervical cancer screening. We also noticed
certain concerns and perceptions of these students regarding future
HPV vaccines and screening programs. In particular, the concern
about side-effects and inadequate information were the two most
cited concerns connected with HPV vaccines and cervical cancer
screening among medical students.
The acceptance of both primary and secondary prevention of
cervical cancer was relatively low in our study. The acceptability of
HPV vaccines was similar to another study (67.8%) among
medical students in India . However, it was lower than
estimates (over 75%) among women in the general population,
government officials, medical personnel in cervical cancer
screening program sites [25,27], and among a small sample of
female college students , but much higher than the 36.2%
among parents of young adolescents , or 40.8% among female
sex workers in China . The acceptability of cervical cancer
screening was similar to that among women in the general
population in a high-incidence area (also a cervical cancer
screening program site) in China  and lower than the 85%
in a small-scale study . The higher acceptability of HPV
vaccines and screening in cervical cancer screening program sites
may partly be explained by years of educational campaigns as part
of government sponsored mass screening programs and thus an
increased knowledge level in these areas. Education programs
among university students and employed women in mainland
China  and among adolescents in Hong Kong  improved
the acceptability of HPV vaccines by about 10%. This emphasizes
the importance of targeted education for cervical cancer in school
Cervical cancer education is relevant also in regards to the poor
knowledge of cervical cancer and its prevention. Fewer than 85%
of medical students knew the right answer to all of the seven
selected knowledge questions in our study. Surprisingly, only
14.4% and 29.0%, respectively, knew that persistent HPV
infection was the necessary cause of cervical cancer and that
there was a prophylactic HPV vaccine available for cervical cancer
in the world. Fewer than 50.0% agreed that cervical cancer could
be prevented by HPV vaccines, while 80.0% thought cervical
cancer could be prevented by screening. All these daunting
statistics point to the lack of necessary education about cervical
cancer prevention for medical students in school. In addition, we
found that a higher level of knowledge was positively associated
with acceptance of HPV vaccines and cervical cancer screening,
which is consistent with findings in other studies in mainland
China [26,27,29,37]. Since the medical students are future care
providers and sources of medical knowledge, their knowledge and
attitudes will directly impact the decisions concerning HPV
vaccination and cervical cancer screening among patients .
Thus, improving medical students knowledge of cervical cancer
appears to be imperative in order to address the barriers to
cervical cancer control programs in China.
In addition to the knowledge level, factors such as gender,
attitude towards premarital sex, and choice of major subject were
important predictors of the acceptability of HPV vaccines and
cervical cancer screening. Female medical students were more
likely to accept vaccines and screening in our study, which is
consistent with the findings for HPV vaccination among health
care providers . Since cervical cancer is a female malignancy,
it is understandable that females may have better understanding of
the disease and thus be more likely to accept prevention. In
another study among parents of young adolescents, mothers were
more reluctant to accept HPV vaccines for their children because
they were more suspicious of newly-developed vaccines . We
found that students with negative or uncertain attitudes towards
premarital sexual behavior are less likely to accept HPV vaccines
or screening compared with those with positive attitudes. This may
be explained by the likelihood that the latter students tend to seek
out sexual health information and consequently know more about
cervical cancer. Since HPV is a sexually transmitted infection,
higher acceptance of HPV vaccines and cervical cancer screening
among those who favor premarital sex is a good sign for
prevention of the infection and cervical cancer. However, another
study showed that women with first experience of sexual
intercourse after the age of 21 years were more likely to receive
screening than those who first had sex at, or before, the age of 20
. This underscores the importance of cervical cancer
education in the early period of college or university for medical
students. In our study, clinical students more readily accepted
cervical cancer than non-clinical medical students, which aligned
well with a similar study among medical students in India .
Obviously, students in clinical medicine are more exposed to
medical courses and other sources of health information.
Perceptions of the timing, target population, and venue for
immunization were explored in our study. 35.4% and 46.4%,
respectively, thought that HPV vaccines ought to be provided at
age 1318 years, junior or senior middle school or equivalent,
which is fairly consistent with the findings in another study among
parents of adolescents . The percentage of students who
preferred vaccines before sexual debut was 65.1%, much higher
than among other population groups in mainland China
[25,26,40] probably due to the overall better knowledge of
cervical cancer among medical students. Over half of the students
thought that HPV vaccines can be given to boys. This is a positive
signal for the possibility of an HPV vaccination program for men
in future in China, because the quadrivalent HPV vaccine for
males has been recommended to prevent genital warts and HPV
transmission by the Advisory Committee on Immunization
Practices in the United States since 2009 . Of course, since
there are uncertainties around the evidence of cost-effectiveness
for vaccination among males in other countries , it is still
early to consider this possibility in China. Consistent with an
earlier study , local CDC was the most-cited venue for
immunization. Although school-based HPV vaccination programs
have been applied in other countries, it might add huge
administrative costs in China where the CDC network is an
existing system for the delivery and management of vaccines .
With wide acceptability, the local CDC can be recommended as a
venue for HPV vaccination in the future. Over half of students
were willing to pay a price lower than 300 RMB (50 USD) for
domestic or imported HPV vaccines, and a much higher
percentage of students would like to receive or recommend
imported vaccines, which might reflect their lack of confidence in
the effectiveness and safety of domestic vaccines . Current
bivalent and quadrivalent vaccines are close to the end of clinical
trial in China, while domestically developed cheaper HPV
vaccines are still at early Phase III trial. Current HPV vaccines
are expensive (about 400 USD for three doses) considering the
average Chinese purchasing power, and they are expected to be
more expensive than domestic vaccines. Earlier studies in other
countries indicate that the price of HPV vaccines is a barrier to
immunization among the population . In addition, 40.9%
of medical students requested price regulation and subsidy for
future HPV vaccine programs. In this regard, heavy subsidies for
HPV vaccines would be required from the government, or
external funding bodies to increase the coverage if they were paid
out of pocket in future.
Perceptions of techniques, onset, interval and pricing of cervical
cancer screening were assessed in this study. To our surprise,
41.4% of medical students did not know any screening techniques;
only 31.6% and 41.1%, respectively, knew the two common
techniques, Pap smear and HPV DNA testing. The fact that these
two techniques are widely used in clinical practice reflects
problems with emphasis on cancer treatment instead of screening
and prevention  and inadequate education in cervical
screening in medical school . The recognition of these
problems can be seen in the recent call for cancer screening
education in Chinese medical schools . It is recommended that
screening should be routinely utilized in women immunized with
full doses of HPV vaccines since the vaccines mainly protect
against cervical cancer attributable to HPV 16/18 . However,
only 72.6% believed that women who have already been
vaccinated require cervical screening. Thus education for cervical
screening is still relevant in China in an era of HPV vaccination.
41.9% and 32% of medical students thought women should start
being screened at 20 years and 25 years, respectively, while 49.2%
and 42.1% considered that screening should be given every year
and two to four years, respectively. Current guidelines in the US
recommend cytology-based screening women aged 21 to 65 years
every three years, or for women aged 30 to 65 years who intend to
increase the interval, concurrent screening with cytology and HPV
DNA testing every five years . In this regard, half of the medical
students had an erroneous belief as to the starting age and interval
for screening. This might be deeply rooted in the practice in
mainland China that many organized health programs such as
employment-based physical examination include annual cervical
screening , partly due to lack of Chinese guidelines for cervical
screening. This gap in practice might be reversed through
education of medical students in school.
There are certain limitations in the study. Firstly, the medical
students surveyed were selected from medical universities or
colleges in southwest China. The results may not be readily
generalizable to the medical students in other areas, since cities in
this part of China are generally less developed economically.
However, since students from both cosmopolitan areas such as
Chengdu and small cities were sampled, the conclusion may reflect
part of the actual medical education scenario. Secondly, since we
did not use a standard validation procedure for the questionnaire
design, information collected might not be completely
representative of actual conditions due to lack of validity and reliability
measures. However, we did carefully incorporate input and
comments from former staff in the field and participants in pilot
surveys in designing the questionnaire, and this transparent
procedure can ensure a relatively reliable and valid questionnaire.
Thirdly, caution should be taken when interpreting the
acceptability of HPV vaccines and cervical cancer screening among
medical students. Acceptability may not necessarily mean that they
will advise use of vaccines in practice. Knowing something good
does not translate into practicing something good. Some factors
that might influence their acceptability such as religion and
concern for promiscuity are not analyzable in current study.
Fourthly, our results only reflect the status quo of current cervical
cancer education for medical students. Most of them may increase
their knowledge rapidly in health care practice. Finally,
constrained by the design, the study might be subject to selection and
information bias due to some participants refusal to participate
and data missing in completing the questionnaires by some
In conclusion, the study indicates low acceptability of HPV
vaccines and cervical cancer screening among medical students.
The acceptability is associated with relevant knowledge, gender,
attitude towards premarital sexual behavior, and the area of major
in a course of medical studies. It is important to improve the
knowledge of HPV and cervical cancer among medical students in
order to supply well-informed health care providers for prevention
and control of cervical cancer.
Figure S1 Supplementary questionnaire: the questionnaire was
used to survey the knowledge and awareness of HPV, cervical
cancer, HPV Vaccines, and cervical cancer screening among
medical students in Southwest China.
We would like to thank fellow students in the Department of Cancer
Epidemiology of the Chinese Academy of Medical Sciences Cancer
Institute for their help in questionnaire design, and students who completed
the questionnaires in the study. We are also grateful to Dr Randeep Gill
and Linda Campbell from the London School of Hygiene and Tropical
Medicine, and Michael Downey from Oxford University for their critical
comments. Part of the work was presented as a poster in 20th World
Congress of Epidemiology (T55) in Anchorage, USA on August 1722,
Conceived and designed the experiments: XFP ZMZ CXY. Performed the
experiments: XFP ZMZ JS FC QLW KL GQS JJZ YW CJF CXY.
Analyzed the data: XFP ZMZ FC YW CJF CXY. Wrote the paper: XFP
1. Ferlay J , Soerjomataram I , Ervik M , Dikshit R , Eser S , et al. ( 2013 ) GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No . 11 [Internet]. Lyon: International Agency for Research on Cancer.
2. Dijkstra MG , Snijders PJ , Arbyn M , Rijkaart DC , Berkhof J , et al. ( 2014 ) Cervical cancer screening: on the way to a shift from cytology to full molecular screening . Ann Oncol 2014 Jan 19 . [Epub ahead of print].
3. Jeronimo J , Bansil P , Lim J , Peck R , Paul P , et al. ( 2014 ) A multicountry evaluation of careHPV testing, visual inspection with acetic acid, and papanicolaou testing for the detection of cervical cancer . Int J Gynecol Cancer 24 : 576 - 585 .
4. Paul P , Winkler JL , Bartolini RM , Penny ME , Huong TT , et al. ( 2013 ) Screenand-treat approach to cervical cancer prevention using visual inspection with acetic acid and cryotherapy: experiences, perceptions, and beliefs from demonstration projects in Peru , Uganda, and Vietnam . Oncologist 18 : 1278 - 1284 .
5. Li R , Zhou Q , Li M , Tong SM , He M , et al. ( 2013 ) Evaluation of visual inspection as the primary screening method in a four-year cervical (pre-) cancer screening program in rural China . Trop Doct 43 : 96 - 99 .
6. Vesco KK , Whitlock EP , Eder M , Burda BU , Senger CA , et al. ( 2011 ) Risk factors and other epidemiologic considerations for cervical cancer screening: a narrative review for the U .S. Preventive Services Task Force . Annals of Internal Medicine 155 : 698 - 705 , W216.
7. WHO ( 2009 ) Human papillomavirus vaccines: WHO position paper . Biologicals 37 : 338 - 344 .
8. Markowitz LE , Tsu V , Deeks SL , Cubie H , Wang SA , et al. ( 2012 ) Human papillomavirus vaccine introduction-the first five years . Vaccine 30 Suppl 5 : F139 - 148 .
9. Brotherton JM , Fridman M , May CL , Chappell G , Saville AM , et al. ( 2011 ) Early effect of the HPV vaccination programme on cervical abnormalities in Victoria, Australia: an ecological study . Lancet 377 : 2085 - 2092 .
10. Kahn JA ( 2009 ) HPV vaccination for the prevention of cervical intraepithelial neoplasia . N Engl J Med 361 : 271 - 278 .
11. Cutts FT , Franceschi S , Goldie S , Castellsague X , de Sanjose S , et al. ( 2007 ) Human papillomavirus and HPV vaccines: a review . Bull World Health Organ 85 : 719 - 726 .
12. Agorastos T , Chatzigeorgiou K , Brotherton JM , Garland SM ( 2009 ) Safety of human papillomavirus (HPV) vaccines: a review of the international experience so far . Vaccine 27 : 7270 - 7281 .
13. Lu B , Kumar A , Castellsague X , Giuliano AR ( 2011 ) Efficacy and safety of prophylactic vaccines against cervical HPV infection and diseases among women: a systematic review & meta-analysis . BMC Infect Dis 11 : 13 .
14. Markowitz LE , Hariri S , Lin C , Dunne EF , Steinau M , et al. ( 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 . J Infect Dis 208 : 385 - 393 .
15. Mesher D , Soldan K , Howell-Jones R , Panwar K , Manyenga P , et al. ( 2013 ) Reduction in HPV 16/18 prevalence in sexually active young women following the introduction of HPV immunisation in England . Vaccine 32 : 26 - 32 .
16. Kavanagh K , Pollock KG , Potts A , Love J , Cuschieri K , et al. ( 2014 ) Introduction and sustained high coverage of the HPV bivalent vaccine leads to a reduction in prevalence of HPV 16/18 and closely related HPV types . Br J Cancer 110 : 2804 - 2811 .
17. Dong Z ( 2005 ) Recommendations for screening, early detection and treatment of cancer in China (draft) . Beijing: Peking University Medical Press .
18. Lancet ( 2009 ) Women's health in rural China . Lancet 374 : 358 .
19. Goss PE , Strasser-Weippl K , Lee-Bychkovsky BL , Fan L , Li J , et al. ( 2014 ) Challenges to effective cancer control in China , India, and Russia . Lancet Oncol 15 : 489 - 538 .
20. Yang L , Parkin DM , Li L , Chen Y ( 2003 ) Time trends in cancer mortality in China: 1987-1999 . Int J Cancer 106 : 771 - 783 .
21. Shi JF , Canfell K , Lew JB , Qiao YL ( 2012 ) The burden of cervical cancer in China: synthesis of the evidence . Int J Cancer 130 : 641 - 652 .
22. Wei MX , Li SW , Huang B , Shen WT , Su YZ , et al. ( 2009 ) [Production of human papillomavirus type 16 virus-like particles and its immunogenicity] . Bing Du Xue Bao 25 : 245 - 250 .
23. Wen Y , Pan XF , Zhao ZM , Chen F , Fu CJ , et al. ( 2014 ) Knowledge of Human Papillomavirus (HPV) Infection, Cervical Cancer, and HPV Vaccine and its Correlates among Medical Students in Southwest China: a Multi-center Crosssectional Survey . Asian Pac J Cancer Prev 15 : 5773 - 5779 .
24. Kuznetsov L , Zippel SA , Ruzicka T , Kuznetsov AV ( 2012 ) Fathers' knowledge of and attitude towards human papillomavirus infection, genitoanal warts, cervical cancer and HPV vaccine . Int J Public Health 57 : 651 - 653 .
25. Li J , Li LK , Ma JF , Wei LH , Niyazi M , et al. ( 2009 ) Knowledge and attitudes about human papillomavirus (HPV) and HPV vaccines among women living in metropolitan and rural regions of China . Vaccine 27 : 1210 - 1215 .
26. Zhang SK , Pan XF , Wang SM , Yang CX , Gao XH , et al. ( 2013 ) Perceptions and acceptability of HPV vaccination among parents of young adolescents: a multicenter national survey in China . Vaccine 31 : 3244 - 3249 .
27. Zhao F-H , Tiggelaar SM , Hu S-Y , Zhao N , Hong Y , et al. ( 2012 ) A Multi-center Survey of HPV Knowledge and Attitudes Toward HPV Vaccination among Women, Government Officials, and Medical Personnel in China . Asian Pacific Journal of Cancer Prevention 13 : 2369 - 2378 .
28. Chang IJ , Huang R , He W , Zhang SK , Wang SM , et al. ( 2013 ) Effect of an educational intervention on HPV knowledge and vaccine attitudes among urban employed women and female undergraduate students in China: a cross-sectional study . BMC Public Health 13 : 916 .
29. Jia Y , Li S , Yang R , Zhou H , Xiang Q , et al. ( 2013 ) Knowledge about cervical cancer and barriers of screening program among women in Wufeng County, a high-incidence region of cervical cancer in China . PLoS One 8 : e67005 .
30. Gu C , Chan CW , Twinn S , Choi KC ( 2012 ) The influence of knowledge and perception of the risk of cervical cancer on screening behavior in mainland Chinese women . Psychooncology 21 : 1299 - 1308 .
31. McCusker SM , Macqueen I , Lough G , Macdonald AI , Campbell C , et al. ( 2013 ) Gaps in detailed knowledge of human papillomavirus (HPV) and the HPV vaccine among medical students in Scotland . BMC Public Health 13 : 264 .
32. Mehta S , Rajaram S , Goel G , Goel N ( 2013 ) Awareness about Human Papilloma Virus and its Vaccine Among Medical Students . Indian J Community Med 38 : 92 - 94 .
33. Pandey D , Vanya V , Bhagat S , Vs B , Shetty J ( 2012 ) Awareness and attitude towards human papillomavirus (HPV) vaccine among medical students in a premier medical school in India . PLoS One 7 : e40619 .
34. Chelimo C , Wouldes TA ( 2009 ) Human papillomavirus knowledge and awareness among undergraduates in healthcare training in New Zealand . N Z Med J 122 : 33 - 45 .
35. Rashwan HH , Saat NZ , Abd Manan DN ( 2012 ) Knowledge, attitude and practice of malaysian medical and pharmacy students towards human papillomavirus vaccination . Asian Pac J Cancer Prev 13 : 2279 - 2283 .
36. Hong Y , Zhang C , Li X , Lin D , Liu Y ( 2013 ) HPV and cervical cancer related knowledge, awareness and testing behaviors in a community sample of female sex workers in China . BMC Public Health 13 : 696 .
37. Gu C , Chan CW , He GP , Choi KC , Yang SB ( 2013 ) Chinese women's motivation to receive future screening: the role of social-demographic factors, knowledge and risk perception of cervical cancer . Eur J Oncol Nurs 17 : 154 - 161 .
38. Kwan TT , Tam KF , Lee PW , Chan KK , Ngan HY ( 2011 ) The effect of schoolbased cervical cancer education on perceptions towards human papillomavirus vaccination among Hong Kong Chinese adolescent girls . Patient Educ Couns 84 : 118 - 122 .
39. Dempsey AF , Davis MM ( 2006 ) Overcoming barriers to adherence to HPV vaccination recommendations . Am J Manag Care 12 : S484 - 491 .
40. Zhao FH , Tiggelaar SM , Hu SY , Xu LN , Hong Y , et al. ( 2012 ) A multi-center survey of age of sexual debut and sexual behavior in Chinese women: suggestions for optimal age of human papillomavirus vaccination in China . Cancer Epidemiol 36 : 384 - 390 .
41. Zimet GD , Rosenthal SL ( 2010 ) HPV vaccine and males: issues and challenges . Gynecol Oncol 117 : S26 - 31 .
42. Kim JJ , Goldie SJ ( 2009 ) Cost effectiveness analysis of including boys in a human papillomavirus vaccination programme in the United States . BMJ 339 : b3884.
43. Chesson HW , Ekwueme DU , Saraiya M , Dunne EF , Markowitz LE ( 2011 ) The cost-effectiveness of male HPV vaccination in the United States . Vaccine 29 : 8443 - 8450 .
44. Jit M , Choi YH , Edmunds WJ ( 2008 ) Economic evaluation of human papillomavirus vaccination in the United Kingdom . BMJ 337 : a769.
45. Zheng J , Zhou Y , Wang H , Liang X ( 2010 ) The role of the China Experts Advisory Committee on Immunization Program . Vaccine 28 Suppl 1: A84 - 87 .
46. Shetty P ( 2014 ) Production: Vaccines from the East . Nature 507 : S12 - 13 .
47. Marek E , Dergez T , Kricskovics A , Kovacs K , Rebek-Nagy G , et al. ( 2011 ) Difficulties in the prevention of cervical cancer: adults' attitudes towards HPV vaccination 3 years after introducing the vaccine in Hungary . Vaccine 29 : 5122 - 5129 .
48. Madhivanan P , Krupp K , Yashodha MN , Marlow L , Klausner JD , et al. ( 2009 ) Attitudes toward HPV vaccination among parents of adolescent girls in Mysore , India. Vaccine 27 : 5203 - 5208 .
49. Sauvageau C , Duval B , Gilca V , Lavoie F , Ouakki M ( 2007 ) Human papilloma virus vaccine and cervical cancer screening acceptability among adults in Quebec, Canada . BMC Public Health 7 : 304 .
50. Deng L , Na FF , Wang JW , Meng MB , He HY , et al. ( 2011 ) Insufficient screening knowledge in Chinese interns: a survey in ten leading medical schools . Asian Pac J Cancer Prev 12 : 2801 - 2806 .
51. Deng L , Na F , Wang J , Lu Y ( 2014 ) Cancer screening education in Chinese medical schools . Lancet Oncol 15 : e300 - 301 .
52. Adams M , Jasani B , Fiander A ( 2007 ) Human papilloma virus (HPV) prophylactic vaccination: challenges for public health and implications for screening . Vaccine 25 : 3007 - 3013 .
53. Gu C , Chan CW , Twinn S ( 2010 ) How sexual history and knowledge of cervical cancer and screening influence Chinese women's screening behavior in mainland China . Cancer Nurs 33 : 445 - 453 .