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Knowledge and attitudes about human papillomavirus (HPV) and HPV vaccines among women living in metropolitan and rural regions of China
Vaccine 27 (2009) 1210–1215
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Knowledge and attitudes about human papillomavirus (HPV) and HPV vaccines among women living in metropolitan and rural regions of China Jing Li a,b , Lian-Kun Li c , Jun-Fei Ma d , Li-Hui Wei e , Mayinuer Niyazi f , Chang-Qing Li g , Ai-Di Xu h , Jian-Bin Wang a , Hao Liang a , Jerome Belinson i , You-Lin Qiao a,∗ a
Department of Cancer Epidemiology, Cancer Institute, Chinese Academy of Medical Sciences, Beijing 100021, China Hormonal and Reproductive Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, 20892 MD, USA Liaoning Provincial Tumor Hospital, Shenyang 110042, China d Xiangyuan Women and Children’s Hospital, Shanxi Province 046200, China e Department of OB/GYN, Peking University People’s Hospital, Beijing 100044, China f Department of OB/GYN, Xinjiang Uygur Autonomous Region Hospital, Urumchi 830001, China g Xinmi Women and Children’s Hospital, Henan Province 452300, China h Hongkou District Women and Children’s Hospital, Shanghai 200082, China i Department of OB/GYN, the Cleveland Clinic Foundation, OH 44195, USA b c
a r t i c l e
i n f o
Article history: Received 20 September 2008 Received in revised form 13 December 2008 Accepted 15 December 2008 Available online 9 January 2009 Keywords: Human papillomavirus (HPV) vaccines Knowledge Acceptability
a b s t r a c t Infection with the human papillomavirus (HPV) is one of the most common sexually transmitted infections and causes virtually all cervical cancer globally. The recent development of two safe and clinically effective vaccines against HPV is a promising step towards lowering cervical cancer rates in the future. What Chinese women think about HPV and the vaccines remains unknown. We undertook a populationbased survey, which was embedded in a cervical cancer screening project and was designed to assess women’s knowledge about HPV and their acceptability to the vaccines. We found that only 15.0% of women in our study reported to have ever heard of HPV, and this knowledge differs by rural (9.3%) and metropolitan areas (21.6%) and also by education. Most (84.6%) participants were willing to be vaccinated if HPV vaccine became available to them. The present study documents ways in which women learn about HPV and indicates the potential barriers and success of introducing HPV vaccine to China. © 2008 Elsevier Ltd. All rights reserved.
1. Introduction Human papillomavirus (HPV), one of the most common sexually transmitted infections, causes virtually all cervical cancer globally. The recent development of two safe and clinically effective vaccines against HPV is a promising step towards lowering cervical cancer rates in the future [1]. Ranked as the second most common cancer among women and the leading cause of death among middle-aged women worldwide, cervical cancer accounts for approximately 500,000 new cases of cancer and 275,000 related deaths annually [1–4]. HPV vaccines have been introduced in many developed countries during recent years with some success. However, in order to achieve significant reduction in worldwide cervical cancer rates, the HPV vaccine will need to be introduced in developing countries, where 80% or more of cervical cancers occur [5].
∗ Corresponding author. Tel.: +86 10 8778 8489; fax: +86 10 6771 3648. E-mail address: [email protected] (Y.-L. Qiao). 0264-410X/$ – see front matter © 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.vaccine.2008.12.020
Two viral like particle (VLP) vaccines have been developed for prophylactic HPV vaccination. Gardasil (Merck and Co., USA) has gained regulatory approval in several countries including the USA. Cervarix (GlaxoSmithKline, Belgium) has been approved in Australia and in the European Union, and applications for approval will be submitted to regulatory agencies in the USA and other countries. Both vaccines target HPV16 and HPV18, which cause approximately 70% of cervical cancer worldwide [4]; Gardasil also targets HPV6 and HPV11, the two HPV types that cause at least 80% of genital warts [6,7]. The clinical efficacy of both HPV vaccines has been established in younger women, and it has been licensed in many developed countries and several developing countries. As China is the largest developing country with cervical cancer mortality increase of 4.1% per year among younger urban females (35–44 years) [8], it is particularly important to understand if any major obstacles to vaccination exist arising from the attitudes of Chinese women. We conducted this survey to better understand women’s knowledge and attitudes about HPV and HPV vaccinations in China.
J. Li et al. / Vaccine 27 (2009) 1210–1215
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2. Material and methods
2.3. Statistical analyses
2.1. Study design and population
Contingency tables using Pearson 2 or Fisher’s exact tests, and tests of trend, were used to establish crude associations of different socio-demographic and behavioral measures. Stratified analyses were used to identify independent determinants of knowledge of HPV. Multivariable logistic regression was used to calculate odds ratios (ORs) and 95% confidence intervals (95%CIs) adjusted for relevant parameters as identified in preliminary data analysis. Specific HPV knowledge among women ever heard of HPV, reasons for willing and unwilling to be vaccinated, acceptable price to pay for the vaccine, source of acceptable recommendation for vaccination, expected suppliers for HPV vaccine and acceptable approaches for payment of the vaccine were calculated simply by number and percentage but stratified by metropolitan or rural inhabitance and years of education (<12 or ≥12 years). SAS statistical software version 9.1 was used to analyze the data. Statistical significance was assessed by two-tailed tests with ˛ level of 0.05.
This survey was questionnaire-based and embedded in a project called “Prevalence Survey of Anogenital Tract HPV Types and Cervix Neoplasia in China”. It was conducted collaboratively by the Cleveland Clinic Foundation (CCF), and the Cancer Institute of the Chinese Academy of Medical Sciences (CICAMS) after approved by the Institutional Review Boards of both organizations. This was a cross-sectional study using non-randomized cluster sampling in geographically and socio-culturally diverse areas of China. A list of 8188 women aged 14–59 years were enumerated from September 2005 to June 2007 from the population lists of 6 community clusters selected respectively from 3 major cities (Shenyang, Shanghai and Beijing) and rural areas in 3 provinces/autonomous regions: Shanxi (Xiangyuan), Xinjiang (Hetian), and Henan (Xinmi). Within each community cluster, quota sampling enrolled approximately 125 women in the 14–19, 20–24, 25–29, 30–34, 35–39, 40–44, 45–49, and 50–59 age groups at each site, or a total about 750 women in each age group. All age-eligible women on the population list were contacted at their homes by local village doctors or town administrators and notified about the study. All mentally and physically competent women aged 14–59 years after providing written, informed consent were eligible for the study regardless of their marital status. Prior to the screening and after informed consent, the participants were administered a risk factor questionnaire that was pre-tested and administered in earlier screening studies of women aged between 35 and 50 years old in Shanxi Province in year 1999 and 2001 [9]. Questions were formulated to explore women’s social-demographic characteristics, sexual and reproductive history, history of doctor diagnosed diseases, family history of cancer, and lifestyle behaviors. A questionnaire of knowledge and attitudes towards cervical cancer, HPV, and HPV vaccines was conducted afterwards. Women were first asked if they had heard of HPV and its related risks. Those who had not were given a basic education by the interviewer prior to continuing the interview. All questions were asked by trained health workers in a confidential setting before the clinical examination. Women then received gynecological examinations in the study clinic situated in their residential district. However, gynecological examination was not carried out on hysterectomized, pregnant and sexually naive women. Cervical and vaginal specimens were collected by doctors from women undergoing the routine exam. Vaginal specimens were obtained from sexually naive women by doctors on a voluntary basis. 2.2. Data collection and quality control Two data input clerks in each site were recruited to double-enter data from the paper to computer-based database (FoxPro) independently after training. All finished double-entry databases were sent to CICAMS for validation by running EpiData. Any inconsistency found by CICAMS between the two databases was reported to the local clerks for adjudication until the databases agreed. As final check, one of databases was chosen and underwent a final consistency check. Logic errors (e.g. a woman reported had never been pregnant yet had more than 1 parity) were again reported back to the local sites, and the local collaborators contacted the participants using the contact information provided in the risk factor questionnaires. After checking with the participants, the local staffs sent the revised database back to CICAMS for final analysis.
3. Results 3.1. Profile of respondents Of the 8188 enumerated women, 89 were not found at the address given on the population list, and 91 were not invited as the required sample size for their age group had been reached. Of the 8008 invited women, 1720 (21.5%) did not accept the invitation to participate in the study, mainly citing that they did not have enough time or did not think they needed a gynecological examination. The proportion of nonparticipation was much larger (32.6%) among women lived in metropolitan than that among women lived in the rural area (7.2%). Thus, we had a starting population sample size of 6288. Of these participants, 262 (4.2%) were not eligible, mainly because they were having their menstruation at their first visit and never came back again. Of all, 6026 (95.8%) met the criteria and 6024 (95.8%) completed the questionnaire; two women from Xinjiang failed to complete the questionnaire because of language barriers. The mean, and age range for the entire population was 34.6 years (SD = 11.7 years) and 14–59 years, respectively. Table 1 reports selected characteristics of the respondents. 3.2. HPV knowledge Of those participating in the study, 15.5% (95%CI = 14.6–16.4%) (931/6024) of women had ever heard of HPV. Fifteen variables were thought to be possibly related to HPV knowledge. After univariate analysis, there were 12 significant associations: HPV Knowledge was greater in women aged 20 and older (13.6–20.0%, depending on 5-year age group) than women under the age of 20 (7.8%); Table 1 Main characteristics of women (N = 6024). Factor
na
Mean or % of na
SD
Range
Age (years) Age at menarche (years) Years of education Age of sexual debut Number of pregnancy Number of live birth Married (%) Never smoker (%) White collar and Professionals (%) Farmers (%) Students (%) Metropolitan inhabitants (%) Rural inhabitants (%)
6024 5808 6026 5002 4228 4778 6024 5801 6023 6023 6023 6024 6024
34.6 15.0 8.0 18.0 3.0 2.0 79.3 92.7 14.0 38.2 14.4 50.0 50.0
11.7 1.9 4.3 8.8 2.5 1.5
14–59 10–26 0–31 9–40 0–7 0–3
a
Number of women out of 6024 interviewed, who answered the question.
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J. Li et al. / Vaccine 27 (2009) 1210–1215
Table 2 Logistic regression models of HPV knowledge. 95% Confidence Interval (95% CI). Item
Ever Heard of HPV n = 931 (%)
Never Heard of HPV n = 5093 (%)
Adjusted-OR (95%CI)
Years of education ≥12 7–12 ≤6
403 (43.29) 244 (26.21) 284 (30.50)
986 (19.36) 2013 (39.52) 2094 (41.12)
1.00 0.45 (0.37–0.55) 0.61 (0.49–0.75)
Previous Pap smear No Yes Not answer
596 (64.02) 288 (30.93) 47 (5.05)
3874 (76.07) 717 (14.08) 502 (9.86)
1.00 2.02 (1.69–2.42) 0.81 (0.57–1.16)
Family member cancer history No Yes Not answer
653 (70.14) 69 (7.41) 209 (22.45)
2660 (44.37) 388 (7.62) 2045 (40.15)
1.00 0.57 (0.43–0.76) 0.65 (0.51–0.82)
Living area Metropolitan Rural
650 (69.82) 281 (30.18)
2361 (46.36) 2732 (53.64)
1.00 0.58 (0.48–0.70)
Sex hygiene (shower before or after sex) 2 351 (37.70) 1 272 (29.22) 0 73 (7.84) Not answer 235 (25.24)
1198 (23.52) 1241 (24.37) 1109 (21.77) 1545 (30.34)
1.00 1.02 (0.84–1.24) 0.40 (0.30–0.53) 0.76 (0.60–0.98)
Urban female (21.6%) were twice as likely to have heard of HPV as those lived in the rural areas (9.3%) (p < 0.0001). Several other factors were significantly associated with HPV knowledge: (1) women who tested HPV negative (vs. HPV positive); (2) previously had a Pap smears (vs. not); (3) history of cervical abnormalities (vs. not); (4) family history of cancer (vs. not); (5) occupation; (6) women with 12 or more years of education (vs. less); (7) women who have never smoked (vs. those who have); (8) alcohol consumption; (9) having had a hysterectomy. There was a significant trend of increasing awareness about HPV with personal hygiene behaviors, as measured by the number of showers (0, 1, or 2) women took before and after having sex. Yet, the rest 3 variables: contraceptive, number of sexual partners in the recent 5 years and marital status were not significantly associated with HPV knowledge.
The multivariable unconditional logistic regression model in Table 2 included those variables that remained significantly associated with HPV knowledge. Women who had less than 12 years of education, had a family history of cancer, lived in a rural area, and took no shower in conjunction with having sex were half as likely to have knowledge about HPV. Women who previously had a Pap smear were twice as knowledgeable about HPV as women who had not. Even among women who had ever heard of HPV (n = 931), specific knowledge about HPV was poor (Table 3). Only 48.2% (449/931) knew that HPV is related to cervical cancer with a higher rate (51.1%) among urban women than that in the rural (41.6%). Even fewer (8.1% (75/931)) knew that it is associated with genital warts with the similar rate in both geographies.
Table 3 Women’s specific HPV knowledge and their acceptable price and source of recommendation for HPV vaccination by living areas and education levels. Item
Metropolitan area All N
%
Rural area
Education <12 years
Education ≥12 years
All
N
N
N
%
(1) When HPV is mentioned, you will firstly think of (n = 931): Cervical cancer 332 51.1 166 43.3 Genital warts 54 8.3 29 7.6 STD 121 18.6 90 23.5 Have no idea about HPV 123 18.9 85 22.2 Others 20 3.1 13 3.4
166 25 31 38 7
Total
267
650
100
383
100
(2) Acceptable price to pay for HPV vaccination (n = 6024) ≤3 US$ 990 32.9 837 34.6 3–7 US$ 944 31.4 795 32.9 7–15 US$ 847 28.1 618 25.6 ≥15 US$ 230 7.6 166 6.9 Not answer 0 0 0 0
153 149 229 64 0
Total
595
3011
100
2416
100
(3)Source of acceptable recommendation for vaccination (n = 6024) Doctors or nurses 1104 36.7 894 37.0 Family members/friends 257 8.5 205 8.5 Hospital open lectures 1391 46.2 1116 46.2 School open lectures 91 3.0 65 2.7 Media (TV/Newspaper) 168 5.6 136 5.6 Not answer 0 0 0 0
210 52 275 26 32 0
Total
595
3011
100
2416
100
% 62.2 9.4 11.6 14.2 2.6 100 25.7 25.0 38.5 10.8 0 100 35.3 8.7 46.2 4.4 5.4 0 100
% 117 21 65 47 31
281 1343 867 474 316 13 3013 1676 92 1106 54 79 6 3013
41.6 7.5 23.1 16.7 11.0 100 44.6 28.8 15.7 10.5 0.4 100 55.6 3.1 36.7 1.8 2.6 0.2 100
Education <12 years
Education ≥12 years
N
N
% 112 19 62 46 31
270 1308 850 465 309 13 2945 1653 88 1075 44 79 6 2945
41.5 7.0 23.0 17.0 11.5 100 44.4 28.9 15.8 10.5 0.4 100 56.1 2.9 36.5 1.5 2.7 0.2 100
5 2 3 1 0 11 35 17 9 7 0 68 23 4 31 10 0 0 68
% 45.5 18.2 27.3 9.1 0 100 51.5 25.0 13.2 10.3 0 100 33.8 5.9 45.6 14.7 0 0 100
J. Li et al. / Vaccine 27 (2009) 1210–1215
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Table 4 Reasons for willing and unwilling to be vaccinated. Item
Metropolitan area All N
%
(1)Reasons for willing to be vaccinated (n = 5099) Self Benefit 255 11.7 Can Benefit other youth 241 11.0 Fear of having cervical cancer 156 7.1 Fear of infecting HPV 257 11.8 Fear of having genital warts 696 31.9 Fear of having been infected 579 26.5 Not answera 1 0.1 Total
2185
100
Rural area Education <12 years
Education ≥12 years
All
N
N
N
186 205 135 186 556 474 1 1743
(2)Reasons for unwilling to be vaccinated (n = 915) I don’t have risk 126 15.3 Don’t think vaccination works 105 12.7 It hasn’t been widely used 85 10.3 Vaccination causes risks 78 9.4 Doubts on the resource 424 51.3 b 8 1.0 Not answer
110 97 58 63 338 7
Total
673
826
100
% 10.8 11.8 7.8 10.7 31.9 27.2 0.1 100 16.3 14.4 8.6 9.4 50.2 1.0 100
69 36 21 71 140 105 0 442 16 8 27 15 86 1 153
% 15.6 8.1 4.8 16.1 31.7 23.8 0 100 10.5 5.2 17.7 9.8 56.2 0.7 100
%
67 38 302 348 498 1649 12 2914 12 8 10 15 38 6 89
2.3 1.0 10.4 11.9 17.1 56.6 0.4 100 13.5 9.0 11.2 16.9 42.7 6.7 100
Education <12 years
Education ≥12 years
N
N
%
67 37 296 346 474 1616 12 2848
2.4 1.3 10.4 12.2 16.6 56.7 0.4 100
11 8 10 15 37 6 87
12.6 9.2 11.5 17.2 42.5 6.9 100
0 1 6 2 24 33 0 66 1 0 0 0 1 0 2
% 0 1.5 9.1 3.0 36.4 50.0 0 100 50.0 0 0 0 50.0 0 100
A total of 6014 women answered they were willing/unwilling to be vaccinated, yet, 10 out of the 6024 interviewed did not give the answer. a Women who answered willing to be vaccinated but did not present the reasons why. b Women who answered unwilling to be vaccinated but did not present the reasons why.
3.3. Attitudes about HPV vaccine Table 4 presents reasons for willing and unwilling to be vaccinated. The majority (84.6%, (95%CI = 83.7–85.6%) (5099/6024)) of participants were willing to be vaccinated. Fear of getting genital warts without vaccination (31.9%; 696/2185) and concern about having been infected with HPV (56.6%; 1649/2914) were the primary reason for urban and rural females to be vaccinated respectively. Doubts on the resources for getting the HPV vaccine (15.4%; 915/6024) was the major reason for unwillingness to get vaccinated, with 42.7% of rural females and 51.3% urban females listing resources as the primary reason (Table 4). Three thousand six hundred and fifty four (60.7%, 3654/6024) women reported that they had daughters. Among them, 86.4% (3156/3654) were willing to vaccinate their daughters, 13% (474/3654) were unwilling, mainly (61.4%, 291/474) because they doubted on the safety of the vaccine, followed by the reason that their daughters were too young to be vaccinated (38.6%, 183/474). Twenty four (0.6%, 24/474) women with daughters did not answer this question. After a simple education about HPV for those unaware about HPV, most of the HPV aware and unaware women expected that the future vaccine can prevent both cervical cancer and genital warts, and the average age they thought would be appropriate to get vaccinated was 19 years old. In addition, 38.7% (2333/6024) women said that would pay less than approximately the equivalent of US$ 3 (20 Renminbi [RMB]), Very few of them (9.1%, 546/6024) would pay more than the equivalent of US$ 15 (100 RMB). Women living in the metropolitan areas were willing to pay more (Table 3). For all women, recommendations from doctors or nurses and hospital lectures were the two major influences in deciding to get vaccinated. Rural females were more likely to rely on the recommendation by doctors or nurses (55.6%, 1676/3013), whereas urban women were more likely to be influenced by hospital lectures 46.2% (1391/3011) (Table 3). Government and medical organization were expected to be the major suppliers for the vaccine other than pharmaceutical companies (Supplemental Online Table 1). And more than half of them
thought that it was the government responsibility to pay for the vaccine or at least pay partly, regardless of where they lived or their education level (Supplemental Online Table 2). 4. Discussion This is the first study to evaluate HPV knowledge and attitudes about HPV vaccine among women in mainland China on a screening basis. It provides useful information for further research and for policy makers. It is clear that HPV awareness is low, and specific knowledge was generally poor even among HPV aware women. This low level of knowledge is consistent with the findings from another study of Chinese women in Hong Kong, which reported 10% of women were aware of HPV but had limited specific knowledge of HPV [10]. In some other countries with well integrated cervical cancer screening program with the Pap test, such as UK and US, the HPV awareness rates were also reported low [11–16]. By contrast, a relatively high rate of HPV awareness (51.2%) was reported in a recent study from Australia, which may due to the increased media coverage, particularly in relation to the development of an HPV vaccination program [17]. As lack of knowledge is regarded as one of the major barriers that pose challenges to widespread implementation of HPV vaccine [18], it becomes essential that significant and sustained public education efforts through the media to raise awareness about HPV and the benefits of HPV immunization will be necessary to ensure a successful application in the future when HPV vaccines are licensed in China. We were able to determine that HPV knowledge was more accessible to women with higher education and those in the metropolitan area. More attention to educating rural populations and less educated populations will be needed in order to increase acceptance of HPV vaccination. A higher HPV awareness level was found in women with previous Pap smear attendance, which maybe the consequence of gaining knowledge from their health care provider during the visit. Increased education of health care providers may increase the general knowledge of HPV in the population. Timely education may help minimize the cost, morbidity and mortality associated with HPV-related dis-
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J. Li et al. / Vaccine 27 (2009) 1210–1215
eases by increasing the participation in screening and vaccination programs. Our findings also suggest that familiarity with HPV does not guarantee accurate knowledge about its link to cervical cancer and genital warts. Thus, when information about HPV is to be delivered, two tasks should be borne in mind: (a) to increase recognition of the name, and (b) to increase the depth of knowledge of the potential consequences of HPV infection. The majority of women were willing to be vaccinated, with a higher percentage in rural women. This is consistent with studies from other areas and countries [10,19,20] and is also similar with the percentage of willingness (86.4%) of mothers to vaccine their daughters. Based on the data collected, fearing of already having been infected was the major reason for them to be vaccinated, which reflects the lack of knowledge about prophylactic vaccines. Doubts on the source of the HPV vaccine and its safety were the major reasons for women’s unwillingness to vaccine themselves and their daughters, among women who would accept vaccination, more than half of them would choose the government supply. This suggests that HPV vaccine must be safety guaranteed and might be best introduced to China through the government-sponsored programs than through any private sectors. As the number of recommended childhood and adolescent vaccines increases and vaccines become increasingly expensive [21,22]. Financing for newly recommended vaccines increasingly may become a barrier to receiving them [18]. At an advertised retail price of US$ 120 per dose (US$ 360 per series) for the quadrivalent HPV vaccine [23], which does not include the administration costs, HPV vaccines are the most expensive vaccine ever [18]. A study in Australia showed that if the cost of HPV vaccine was more than US$ 200, mothers became more reluctant to vaccine their daughters [24]. In our study, 79% women expect that the government pays or at least partly covers the cost of the vaccine and almost 70% of them were willing to pay less than US$ 7 for the vaccine if they have to, which shows a huge gap between the asking and acceptable price of HPV vaccination. The introductory price will need to be drastically lowered through government programs, tiered pricing of the vaccine by pharmaceutical companies, and/or donors in order to make the vaccine available and acceptable to Chinese women. Although women reported several sources of acceptable recommendations for vaccination, they demonstrated very high levels of trust in doctors or nurses and hospital lectures. Rural female preferred the former, and the urban tended to prefer the latter; indicating that a recommendation to vaccinate them or their daughters against HPV would be most effective if delivered by health professionals. In conclusion, the HPV awareness is low in Chinese women, yet the acceptability to its vaccine is high if the price and safety are guaranteed. Education level and living area are the major factors that are related to the HPV awareness. Health care providers and hospital lectures should play an important role to deliver knowledge about HPV and its vaccine in the rural and the metropolitan areas respectively. Scientific but simplified reports from media should also be encouraged. Factors that are essential to the successful implementation of HPV vaccine to China will be widespread public health campaign about HPV and the vaccine, government buy-in with commitment of resources, affordable vaccines, and the establishment of a health infrastructure especially in the rural areas for vaccine delivery. Acknowledgements This study was supported by Cleveland Clinic Foundation (CCF) through fixed price contract.
We thank the Cancer Foundation of China (CFC) and the Cancer Institute of the Chinese Academy of Medical Sciences (CICAMS) with providing their expertise in the development of the study. We also thank the local health workers from Beijing, Shanghai, Shenyang, Shanxi (Xiangyuan), Xinjiang (Hetian), and Henan (Xinmi) for inviting women to participate in the study and assisting us complete the project successfully. The authors thank Dr. Philip Castle (U.S. National Cancer Institute, NIH, DHHS) for his help with the data analysis and manuscript preparation. Dr. Jing Li was supported by the Hormonal and Reproductive Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, DHHS and the Short Term Scientist Exchange Program (STSEP) from the National Institute of Health (NIH). Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.vaccine.2008.12.020. References [1] Trottier H, Franco EL. The epidemiology of genital human papillomavirus infection. Vaccine 2006;24(March (Suppl. 1)):S1–15. [2] Schiffman M, Castle PE. Human papillomavirus: epidemiology and public health. Arch Pathol Lab Med 2003;127(August (8)):930–4. [3] Franco EL, Harper DM. Vaccination against human papillomavirus infection: a new paradigm in cervical cancer control. Vaccine 2005;23(March (17–18)):2388–94. [4] Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003;348(February (6)):518–27. [5] International Agency for Research on Cancer. Human Papillomaviruses. IARC Monographs on the evaluation of carcinogenic risks to humans, vol. 64. Lyon (FRC): IARC Press; 1995. [6] Greer CE, Wheeler CM, Ladner MB, Beutner K, Coyne MY, Liang H, et al. Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus-like particles in patients with genital warts. J Clin Microbiol 1995;33(August (8)):2058–63. [7] Li HX, Zhu WY, Xia MY. Detection with the polymerase chain reaction of human papillomavirus DNA in condylomata acuminata treated with CO2 laser and microwave. Int J Dermatol 1995;34(March (3)):209–11. [8] Yang L, Parkin DM, Li L, Chen Y. Time trends in cancer mortality in China: 1987–1999. Int J Cancer 2003;106(September (5)):771–83. [9] Rong S, Chen W, Wu L, Zhang X, Shen G, Liu Y, et al. Analysis of risk factors for cervical cancer in Xiangyuan County, Shanxi Province. Zhonghua Yu Fang Yi Xue Za Zhi 2002;36(January (1)):41–3. [10] Lee Peter WH, Kwan Tracy TC, Tam Kar Fai, Chan Karen KL, Young Phyllis MC, Lo Sue ST, et al. Beliefs about cervical cancer and human papillomavirus (HPV) and acceptability of HPV vaccination among Chinese women in Hong Kong. Prev Med 2007;45(2–3):130–4. [11] Vail-Smith K, White DM. Risk level, knowledge, and preventive behavior for human papillomaviruses among sexually active college women. J Am Coll Health 1992;40(March (5)):227–30. [12] Mays RM, Zimet GD, Winston Y, Kee R, Dickes J, Su L. Human papillomavirus, genital warts, Pap smears, and cervical cancer: knowledge and beliefs of adolescent and adult women. Health Care Women Int 2000;21(July–August (5)):361–74. [13] Dell DL, Chen H, Ahmad F, Stewart DE. Knowledge about human papillomavirus among adolescents. Obstet Gynecol 2000;96(November (5 Pt 1)): 653–6. [14] Marlow LA, Waller J, Wardle J. Public awareness that HPV is a risk factor for cervical cancer. Br J Cancer 2007;97(September (5)):691–4. [15] Pitts M, Clarke T. Human papillomavirus infections and risks of cervical cancer: what do women know? Health Educ Res 2002;17(December (6)): 706–14. [16] Tiro JA, Meissner HI, Kobrin S, Chollette V. What do women in the U.S. know about human papillomavirus and cervical cancer? Cancer Epidemiol Biomarkers Prev 2007;16(February (2)):288–94. [17] Pitts MK, Dyson SJ, Rosenthal DA, Garland SM. Knowledge and awareness of human papillomavirus (HPV): attitudes towards HPV vaccination among a representative sample of women in Victoria, Australia. Sex Health 2007;4(September (3)):177–80. [18] Dempsey AF, Davis MM. Overcoming barriers to adherence to HPV vaccination recommendations. Am J Manage Care 2006;12(December (17 Suppl.)): S484–91. [19] Brabin L, Roberts SA, Farzaneh F, Kitchener HC. Future acceptance of adolescent human papillomavirus vaccination: a survey of parental attitudes. Vaccine 2006;24(April (16)):3087–94. [20] Woodhall SC, Lehtinen M, Verho T, Huhtala H, Hokkanen M, Kosunen E. Anticipated acceptance of HPV vaccination at the baseline of implementation: a
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Vaccine journal homepage: www.elsevier.com/locate/vaccine
Knowledge and attitudes about human papillomavirus (HPV) and HPV vaccines among women living in metropolitan and rural regions of China Jing Li a,b , Lian-Kun Li c , Jun-Fei Ma d , Li-Hui Wei e , Mayinuer Niyazi f , Chang-Qing Li g , Ai-Di Xu h , Jian-Bin Wang a , Hao Liang a , Jerome Belinson i , You-Lin Qiao a,∗ a
Department of Cancer Epidemiology, Cancer Institute, Chinese Academy of Medical Sciences, Beijing 100021, China Hormonal and Reproductive Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, 20892 MD, USA Liaoning Provincial Tumor Hospital, Shenyang 110042, China d Xiangyuan Women and Children’s Hospital, Shanxi Province 046200, China e Department of OB/GYN, Peking University People’s Hospital, Beijing 100044, China f Department of OB/GYN, Xinjiang Uygur Autonomous Region Hospital, Urumchi 830001, China g Xinmi Women and Children’s Hospital, Henan Province 452300, China h Hongkou District Women and Children’s Hospital, Shanghai 200082, China i Department of OB/GYN, the Cleveland Clinic Foundation, OH 44195, USA b c
a r t i c l e
i n f o
Article history: Received 20 September 2008 Received in revised form 13 December 2008 Accepted 15 December 2008 Available online 9 January 2009 Keywords: Human papillomavirus (HPV) vaccines Knowledge Acceptability
a b s t r a c t Infection with the human papillomavirus (HPV) is one of the most common sexually transmitted infections and causes virtually all cervical cancer globally. The recent development of two safe and clinically effective vaccines against HPV is a promising step towards lowering cervical cancer rates in the future. What Chinese women think about HPV and the vaccines remains unknown. We undertook a populationbased survey, which was embedded in a cervical cancer screening project and was designed to assess women’s knowledge about HPV and their acceptability to the vaccines. We found that only 15.0% of women in our study reported to have ever heard of HPV, and this knowledge differs by rural (9.3%) and metropolitan areas (21.6%) and also by education. Most (84.6%) participants were willing to be vaccinated if HPV vaccine became available to them. The present study documents ways in which women learn about HPV and indicates the potential barriers and success of introducing HPV vaccine to China. © 2008 Elsevier Ltd. All rights reserved.
1. Introduction Human papillomavirus (HPV), one of the most common sexually transmitted infections, causes virtually all cervical cancer globally. The recent development of two safe and clinically effective vaccines against HPV is a promising step towards lowering cervical cancer rates in the future [1]. Ranked as the second most common cancer among women and the leading cause of death among middle-aged women worldwide, cervical cancer accounts for approximately 500,000 new cases of cancer and 275,000 related deaths annually [1–4]. HPV vaccines have been introduced in many developed countries during recent years with some success. However, in order to achieve significant reduction in worldwide cervical cancer rates, the HPV vaccine will need to be introduced in developing countries, where 80% or more of cervical cancers occur [5].
∗ Corresponding author. Tel.: +86 10 8778 8489; fax: +86 10 6771 3648. E-mail address: [email protected] (Y.-L. Qiao). 0264-410X/$ – see front matter © 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.vaccine.2008.12.020
Two viral like particle (VLP) vaccines have been developed for prophylactic HPV vaccination. Gardasil (Merck and Co., USA) has gained regulatory approval in several countries including the USA. Cervarix (GlaxoSmithKline, Belgium) has been approved in Australia and in the European Union, and applications for approval will be submitted to regulatory agencies in the USA and other countries. Both vaccines target HPV16 and HPV18, which cause approximately 70% of cervical cancer worldwide [4]; Gardasil also targets HPV6 and HPV11, the two HPV types that cause at least 80% of genital warts [6,7]. The clinical efficacy of both HPV vaccines has been established in younger women, and it has been licensed in many developed countries and several developing countries. As China is the largest developing country with cervical cancer mortality increase of 4.1% per year among younger urban females (35–44 years) [8], it is particularly important to understand if any major obstacles to vaccination exist arising from the attitudes of Chinese women. We conducted this survey to better understand women’s knowledge and attitudes about HPV and HPV vaccinations in China.
J. Li et al. / Vaccine 27 (2009) 1210–1215
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2. Material and methods
2.3. Statistical analyses
2.1. Study design and population
Contingency tables using Pearson 2 or Fisher’s exact tests, and tests of trend, were used to establish crude associations of different socio-demographic and behavioral measures. Stratified analyses were used to identify independent determinants of knowledge of HPV. Multivariable logistic regression was used to calculate odds ratios (ORs) and 95% confidence intervals (95%CIs) adjusted for relevant parameters as identified in preliminary data analysis. Specific HPV knowledge among women ever heard of HPV, reasons for willing and unwilling to be vaccinated, acceptable price to pay for the vaccine, source of acceptable recommendation for vaccination, expected suppliers for HPV vaccine and acceptable approaches for payment of the vaccine were calculated simply by number and percentage but stratified by metropolitan or rural inhabitance and years of education (<12 or ≥12 years). SAS statistical software version 9.1 was used to analyze the data. Statistical significance was assessed by two-tailed tests with ˛ level of 0.05.
This survey was questionnaire-based and embedded in a project called “Prevalence Survey of Anogenital Tract HPV Types and Cervix Neoplasia in China”. It was conducted collaboratively by the Cleveland Clinic Foundation (CCF), and the Cancer Institute of the Chinese Academy of Medical Sciences (CICAMS) after approved by the Institutional Review Boards of both organizations. This was a cross-sectional study using non-randomized cluster sampling in geographically and socio-culturally diverse areas of China. A list of 8188 women aged 14–59 years were enumerated from September 2005 to June 2007 from the population lists of 6 community clusters selected respectively from 3 major cities (Shenyang, Shanghai and Beijing) and rural areas in 3 provinces/autonomous regions: Shanxi (Xiangyuan), Xinjiang (Hetian), and Henan (Xinmi). Within each community cluster, quota sampling enrolled approximately 125 women in the 14–19, 20–24, 25–29, 30–34, 35–39, 40–44, 45–49, and 50–59 age groups at each site, or a total about 750 women in each age group. All age-eligible women on the population list were contacted at their homes by local village doctors or town administrators and notified about the study. All mentally and physically competent women aged 14–59 years after providing written, informed consent were eligible for the study regardless of their marital status. Prior to the screening and after informed consent, the participants were administered a risk factor questionnaire that was pre-tested and administered in earlier screening studies of women aged between 35 and 50 years old in Shanxi Province in year 1999 and 2001 [9]. Questions were formulated to explore women’s social-demographic characteristics, sexual and reproductive history, history of doctor diagnosed diseases, family history of cancer, and lifestyle behaviors. A questionnaire of knowledge and attitudes towards cervical cancer, HPV, and HPV vaccines was conducted afterwards. Women were first asked if they had heard of HPV and its related risks. Those who had not were given a basic education by the interviewer prior to continuing the interview. All questions were asked by trained health workers in a confidential setting before the clinical examination. Women then received gynecological examinations in the study clinic situated in their residential district. However, gynecological examination was not carried out on hysterectomized, pregnant and sexually naive women. Cervical and vaginal specimens were collected by doctors from women undergoing the routine exam. Vaginal specimens were obtained from sexually naive women by doctors on a voluntary basis. 2.2. Data collection and quality control Two data input clerks in each site were recruited to double-enter data from the paper to computer-based database (FoxPro) independently after training. All finished double-entry databases were sent to CICAMS for validation by running EpiData. Any inconsistency found by CICAMS between the two databases was reported to the local clerks for adjudication until the databases agreed. As final check, one of databases was chosen and underwent a final consistency check. Logic errors (e.g. a woman reported had never been pregnant yet had more than 1 parity) were again reported back to the local sites, and the local collaborators contacted the participants using the contact information provided in the risk factor questionnaires. After checking with the participants, the local staffs sent the revised database back to CICAMS for final analysis.
3. Results 3.1. Profile of respondents Of the 8188 enumerated women, 89 were not found at the address given on the population list, and 91 were not invited as the required sample size for their age group had been reached. Of the 8008 invited women, 1720 (21.5%) did not accept the invitation to participate in the study, mainly citing that they did not have enough time or did not think they needed a gynecological examination. The proportion of nonparticipation was much larger (32.6%) among women lived in metropolitan than that among women lived in the rural area (7.2%). Thus, we had a starting population sample size of 6288. Of these participants, 262 (4.2%) were not eligible, mainly because they were having their menstruation at their first visit and never came back again. Of all, 6026 (95.8%) met the criteria and 6024 (95.8%) completed the questionnaire; two women from Xinjiang failed to complete the questionnaire because of language barriers. The mean, and age range for the entire population was 34.6 years (SD = 11.7 years) and 14–59 years, respectively. Table 1 reports selected characteristics of the respondents. 3.2. HPV knowledge Of those participating in the study, 15.5% (95%CI = 14.6–16.4%) (931/6024) of women had ever heard of HPV. Fifteen variables were thought to be possibly related to HPV knowledge. After univariate analysis, there were 12 significant associations: HPV Knowledge was greater in women aged 20 and older (13.6–20.0%, depending on 5-year age group) than women under the age of 20 (7.8%); Table 1 Main characteristics of women (N = 6024). Factor
na
Mean or % of na
SD
Range
Age (years) Age at menarche (years) Years of education Age of sexual debut Number of pregnancy Number of live birth Married (%) Never smoker (%) White collar and Professionals (%) Farmers (%) Students (%) Metropolitan inhabitants (%) Rural inhabitants (%)
6024 5808 6026 5002 4228 4778 6024 5801 6023 6023 6023 6024 6024
34.6 15.0 8.0 18.0 3.0 2.0 79.3 92.7 14.0 38.2 14.4 50.0 50.0
11.7 1.9 4.3 8.8 2.5 1.5
14–59 10–26 0–31 9–40 0–7 0–3
a
Number of women out of 6024 interviewed, who answered the question.
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J. Li et al. / Vaccine 27 (2009) 1210–1215
Table 2 Logistic regression models of HPV knowledge. 95% Confidence Interval (95% CI). Item
Ever Heard of HPV n = 931 (%)
Never Heard of HPV n = 5093 (%)
Adjusted-OR (95%CI)
Years of education ≥12 7–12 ≤6
403 (43.29) 244 (26.21) 284 (30.50)
986 (19.36) 2013 (39.52) 2094 (41.12)
1.00 0.45 (0.37–0.55) 0.61 (0.49–0.75)
Previous Pap smear No Yes Not answer
596 (64.02) 288 (30.93) 47 (5.05)
3874 (76.07) 717 (14.08) 502 (9.86)
1.00 2.02 (1.69–2.42) 0.81 (0.57–1.16)
Family member cancer history No Yes Not answer
653 (70.14) 69 (7.41) 209 (22.45)
2660 (44.37) 388 (7.62) 2045 (40.15)
1.00 0.57 (0.43–0.76) 0.65 (0.51–0.82)
Living area Metropolitan Rural
650 (69.82) 281 (30.18)
2361 (46.36) 2732 (53.64)
1.00 0.58 (0.48–0.70)
Sex hygiene (shower before or after sex) 2 351 (37.70) 1 272 (29.22) 0 73 (7.84) Not answer 235 (25.24)
1198 (23.52) 1241 (24.37) 1109 (21.77) 1545 (30.34)
1.00 1.02 (0.84–1.24) 0.40 (0.30–0.53) 0.76 (0.60–0.98)
Urban female (21.6%) were twice as likely to have heard of HPV as those lived in the rural areas (9.3%) (p < 0.0001). Several other factors were significantly associated with HPV knowledge: (1) women who tested HPV negative (vs. HPV positive); (2) previously had a Pap smears (vs. not); (3) history of cervical abnormalities (vs. not); (4) family history of cancer (vs. not); (5) occupation; (6) women with 12 or more years of education (vs. less); (7) women who have never smoked (vs. those who have); (8) alcohol consumption; (9) having had a hysterectomy. There was a significant trend of increasing awareness about HPV with personal hygiene behaviors, as measured by the number of showers (0, 1, or 2) women took before and after having sex. Yet, the rest 3 variables: contraceptive, number of sexual partners in the recent 5 years and marital status were not significantly associated with HPV knowledge.
The multivariable unconditional logistic regression model in Table 2 included those variables that remained significantly associated with HPV knowledge. Women who had less than 12 years of education, had a family history of cancer, lived in a rural area, and took no shower in conjunction with having sex were half as likely to have knowledge about HPV. Women who previously had a Pap smear were twice as knowledgeable about HPV as women who had not. Even among women who had ever heard of HPV (n = 931), specific knowledge about HPV was poor (Table 3). Only 48.2% (449/931) knew that HPV is related to cervical cancer with a higher rate (51.1%) among urban women than that in the rural (41.6%). Even fewer (8.1% (75/931)) knew that it is associated with genital warts with the similar rate in both geographies.
Table 3 Women’s specific HPV knowledge and their acceptable price and source of recommendation for HPV vaccination by living areas and education levels. Item
Metropolitan area All N
%
Rural area
Education <12 years
Education ≥12 years
All
N
N
N
%
(1) When HPV is mentioned, you will firstly think of (n = 931): Cervical cancer 332 51.1 166 43.3 Genital warts 54 8.3 29 7.6 STD 121 18.6 90 23.5 Have no idea about HPV 123 18.9 85 22.2 Others 20 3.1 13 3.4
166 25 31 38 7
Total
267
650
100
383
100
(2) Acceptable price to pay for HPV vaccination (n = 6024) ≤3 US$ 990 32.9 837 34.6 3–7 US$ 944 31.4 795 32.9 7–15 US$ 847 28.1 618 25.6 ≥15 US$ 230 7.6 166 6.9 Not answer 0 0 0 0
153 149 229 64 0
Total
595
3011
100
2416
100
(3)Source of acceptable recommendation for vaccination (n = 6024) Doctors or nurses 1104 36.7 894 37.0 Family members/friends 257 8.5 205 8.5 Hospital open lectures 1391 46.2 1116 46.2 School open lectures 91 3.0 65 2.7 Media (TV/Newspaper) 168 5.6 136 5.6 Not answer 0 0 0 0
210 52 275 26 32 0
Total
595
3011
100
2416
100
% 62.2 9.4 11.6 14.2 2.6 100 25.7 25.0 38.5 10.8 0 100 35.3 8.7 46.2 4.4 5.4 0 100
% 117 21 65 47 31
281 1343 867 474 316 13 3013 1676 92 1106 54 79 6 3013
41.6 7.5 23.1 16.7 11.0 100 44.6 28.8 15.7 10.5 0.4 100 55.6 3.1 36.7 1.8 2.6 0.2 100
Education <12 years
Education ≥12 years
N
N
% 112 19 62 46 31
270 1308 850 465 309 13 2945 1653 88 1075 44 79 6 2945
41.5 7.0 23.0 17.0 11.5 100 44.4 28.9 15.8 10.5 0.4 100 56.1 2.9 36.5 1.5 2.7 0.2 100
5 2 3 1 0 11 35 17 9 7 0 68 23 4 31 10 0 0 68
% 45.5 18.2 27.3 9.1 0 100 51.5 25.0 13.2 10.3 0 100 33.8 5.9 45.6 14.7 0 0 100
J. Li et al. / Vaccine 27 (2009) 1210–1215
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Table 4 Reasons for willing and unwilling to be vaccinated. Item
Metropolitan area All N
%
(1)Reasons for willing to be vaccinated (n = 5099) Self Benefit 255 11.7 Can Benefit other youth 241 11.0 Fear of having cervical cancer 156 7.1 Fear of infecting HPV 257 11.8 Fear of having genital warts 696 31.9 Fear of having been infected 579 26.5 Not answera 1 0.1 Total
2185
100
Rural area Education <12 years
Education ≥12 years
All
N
N
N
186 205 135 186 556 474 1 1743
(2)Reasons for unwilling to be vaccinated (n = 915) I don’t have risk 126 15.3 Don’t think vaccination works 105 12.7 It hasn’t been widely used 85 10.3 Vaccination causes risks 78 9.4 Doubts on the resource 424 51.3 b 8 1.0 Not answer
110 97 58 63 338 7
Total
673
826
100
% 10.8 11.8 7.8 10.7 31.9 27.2 0.1 100 16.3 14.4 8.6 9.4 50.2 1.0 100
69 36 21 71 140 105 0 442 16 8 27 15 86 1 153
% 15.6 8.1 4.8 16.1 31.7 23.8 0 100 10.5 5.2 17.7 9.8 56.2 0.7 100
%
67 38 302 348 498 1649 12 2914 12 8 10 15 38 6 89
2.3 1.0 10.4 11.9 17.1 56.6 0.4 100 13.5 9.0 11.2 16.9 42.7 6.7 100
Education <12 years
Education ≥12 years
N
N
%
67 37 296 346 474 1616 12 2848
2.4 1.3 10.4 12.2 16.6 56.7 0.4 100
11 8 10 15 37 6 87
12.6 9.2 11.5 17.2 42.5 6.9 100
0 1 6 2 24 33 0 66 1 0 0 0 1 0 2
% 0 1.5 9.1 3.0 36.4 50.0 0 100 50.0 0 0 0 50.0 0 100
A total of 6014 women answered they were willing/unwilling to be vaccinated, yet, 10 out of the 6024 interviewed did not give the answer. a Women who answered willing to be vaccinated but did not present the reasons why. b Women who answered unwilling to be vaccinated but did not present the reasons why.
3.3. Attitudes about HPV vaccine Table 4 presents reasons for willing and unwilling to be vaccinated. The majority (84.6%, (95%CI = 83.7–85.6%) (5099/6024)) of participants were willing to be vaccinated. Fear of getting genital warts without vaccination (31.9%; 696/2185) and concern about having been infected with HPV (56.6%; 1649/2914) were the primary reason for urban and rural females to be vaccinated respectively. Doubts on the resources for getting the HPV vaccine (15.4%; 915/6024) was the major reason for unwillingness to get vaccinated, with 42.7% of rural females and 51.3% urban females listing resources as the primary reason (Table 4). Three thousand six hundred and fifty four (60.7%, 3654/6024) women reported that they had daughters. Among them, 86.4% (3156/3654) were willing to vaccinate their daughters, 13% (474/3654) were unwilling, mainly (61.4%, 291/474) because they doubted on the safety of the vaccine, followed by the reason that their daughters were too young to be vaccinated (38.6%, 183/474). Twenty four (0.6%, 24/474) women with daughters did not answer this question. After a simple education about HPV for those unaware about HPV, most of the HPV aware and unaware women expected that the future vaccine can prevent both cervical cancer and genital warts, and the average age they thought would be appropriate to get vaccinated was 19 years old. In addition, 38.7% (2333/6024) women said that would pay less than approximately the equivalent of US$ 3 (20 Renminbi [RMB]), Very few of them (9.1%, 546/6024) would pay more than the equivalent of US$ 15 (100 RMB). Women living in the metropolitan areas were willing to pay more (Table 3). For all women, recommendations from doctors or nurses and hospital lectures were the two major influences in deciding to get vaccinated. Rural females were more likely to rely on the recommendation by doctors or nurses (55.6%, 1676/3013), whereas urban women were more likely to be influenced by hospital lectures 46.2% (1391/3011) (Table 3). Government and medical organization were expected to be the major suppliers for the vaccine other than pharmaceutical companies (Supplemental Online Table 1). And more than half of them
thought that it was the government responsibility to pay for the vaccine or at least pay partly, regardless of where they lived or their education level (Supplemental Online Table 2). 4. Discussion This is the first study to evaluate HPV knowledge and attitudes about HPV vaccine among women in mainland China on a screening basis. It provides useful information for further research and for policy makers. It is clear that HPV awareness is low, and specific knowledge was generally poor even among HPV aware women. This low level of knowledge is consistent with the findings from another study of Chinese women in Hong Kong, which reported 10% of women were aware of HPV but had limited specific knowledge of HPV [10]. In some other countries with well integrated cervical cancer screening program with the Pap test, such as UK and US, the HPV awareness rates were also reported low [11–16]. By contrast, a relatively high rate of HPV awareness (51.2%) was reported in a recent study from Australia, which may due to the increased media coverage, particularly in relation to the development of an HPV vaccination program [17]. As lack of knowledge is regarded as one of the major barriers that pose challenges to widespread implementation of HPV vaccine [18], it becomes essential that significant and sustained public education efforts through the media to raise awareness about HPV and the benefits of HPV immunization will be necessary to ensure a successful application in the future when HPV vaccines are licensed in China. We were able to determine that HPV knowledge was more accessible to women with higher education and those in the metropolitan area. More attention to educating rural populations and less educated populations will be needed in order to increase acceptance of HPV vaccination. A higher HPV awareness level was found in women with previous Pap smear attendance, which maybe the consequence of gaining knowledge from their health care provider during the visit. Increased education of health care providers may increase the general knowledge of HPV in the population. Timely education may help minimize the cost, morbidity and mortality associated with HPV-related dis-
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eases by increasing the participation in screening and vaccination programs. Our findings also suggest that familiarity with HPV does not guarantee accurate knowledge about its link to cervical cancer and genital warts. Thus, when information about HPV is to be delivered, two tasks should be borne in mind: (a) to increase recognition of the name, and (b) to increase the depth of knowledge of the potential consequences of HPV infection. The majority of women were willing to be vaccinated, with a higher percentage in rural women. This is consistent with studies from other areas and countries [10,19,20] and is also similar with the percentage of willingness (86.4%) of mothers to vaccine their daughters. Based on the data collected, fearing of already having been infected was the major reason for them to be vaccinated, which reflects the lack of knowledge about prophylactic vaccines. Doubts on the source of the HPV vaccine and its safety were the major reasons for women’s unwillingness to vaccine themselves and their daughters, among women who would accept vaccination, more than half of them would choose the government supply. This suggests that HPV vaccine must be safety guaranteed and might be best introduced to China through the government-sponsored programs than through any private sectors. As the number of recommended childhood and adolescent vaccines increases and vaccines become increasingly expensive [21,22]. Financing for newly recommended vaccines increasingly may become a barrier to receiving them [18]. At an advertised retail price of US$ 120 per dose (US$ 360 per series) for the quadrivalent HPV vaccine [23], which does not include the administration costs, HPV vaccines are the most expensive vaccine ever [18]. A study in Australia showed that if the cost of HPV vaccine was more than US$ 200, mothers became more reluctant to vaccine their daughters [24]. In our study, 79% women expect that the government pays or at least partly covers the cost of the vaccine and almost 70% of them were willing to pay less than US$ 7 for the vaccine if they have to, which shows a huge gap between the asking and acceptable price of HPV vaccination. The introductory price will need to be drastically lowered through government programs, tiered pricing of the vaccine by pharmaceutical companies, and/or donors in order to make the vaccine available and acceptable to Chinese women. Although women reported several sources of acceptable recommendations for vaccination, they demonstrated very high levels of trust in doctors or nurses and hospital lectures. Rural female preferred the former, and the urban tended to prefer the latter; indicating that a recommendation to vaccinate them or their daughters against HPV would be most effective if delivered by health professionals. In conclusion, the HPV awareness is low in Chinese women, yet the acceptability to its vaccine is high if the price and safety are guaranteed. Education level and living area are the major factors that are related to the HPV awareness. Health care providers and hospital lectures should play an important role to deliver knowledge about HPV and its vaccine in the rural and the metropolitan areas respectively. Scientific but simplified reports from media should also be encouraged. Factors that are essential to the successful implementation of HPV vaccine to China will be widespread public health campaign about HPV and the vaccine, government buy-in with commitment of resources, affordable vaccines, and the establishment of a health infrastructure especially in the rural areas for vaccine delivery. Acknowledgements This study was supported by Cleveland Clinic Foundation (CCF) through fixed price contract.
We thank the Cancer Foundation of China (CFC) and the Cancer Institute of the Chinese Academy of Medical Sciences (CICAMS) with providing their expertise in the development of the study. We also thank the local health workers from Beijing, Shanghai, Shenyang, Shanxi (Xiangyuan), Xinjiang (Hetian), and Henan (Xinmi) for inviting women to participate in the study and assisting us complete the project successfully. The authors thank Dr. Philip Castle (U.S. National Cancer Institute, NIH, DHHS) for his help with the data analysis and manuscript preparation. Dr. Jing Li was supported by the Hormonal and Reproductive Epidemiology Branch, Division of Cancer Epidemiology and Genetics, National Cancer Institute, NIH, DHHS and the Short Term Scientist Exchange Program (STSEP) from the National Institute of Health (NIH). Appendix A. Supplementary data Supplementary data associated with this article can be found, in the online version, at doi:10.1016/j.vaccine.2008.12.020. References [1] Trottier H, Franco EL. The epidemiology of genital human papillomavirus infection. Vaccine 2006;24(March (Suppl. 1)):S1–15. [2] Schiffman M, Castle PE. Human papillomavirus: epidemiology and public health. Arch Pathol Lab Med 2003;127(August (8)):930–4. [3] Franco EL, Harper DM. Vaccination against human papillomavirus infection: a new paradigm in cervical cancer control. Vaccine 2005;23(March (17–18)):2388–94. [4] Munoz N, Bosch FX, de Sanjose S, Herrero R, Castellsague X, Shah KV, et al. Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003;348(February (6)):518–27. [5] International Agency for Research on Cancer. Human Papillomaviruses. IARC Monographs on the evaluation of carcinogenic risks to humans, vol. 64. Lyon (FRC): IARC Press; 1995. [6] Greer CE, Wheeler CM, Ladner MB, Beutner K, Coyne MY, Liang H, et al. Human papillomavirus (HPV) type distribution and serological response to HPV type 6 virus-like particles in patients with genital warts. J Clin Microbiol 1995;33(August (8)):2058–63. [7] Li HX, Zhu WY, Xia MY. Detection with the polymerase chain reaction of human papillomavirus DNA in condylomata acuminata treated with CO2 laser and microwave. Int J Dermatol 1995;34(March (3)):209–11. [8] Yang L, Parkin DM, Li L, Chen Y. Time trends in cancer mortality in China: 1987–1999. Int J Cancer 2003;106(September (5)):771–83. [9] Rong S, Chen W, Wu L, Zhang X, Shen G, Liu Y, et al. Analysis of risk factors for cervical cancer in Xiangyuan County, Shanxi Province. Zhonghua Yu Fang Yi Xue Za Zhi 2002;36(January (1)):41–3. [10] Lee Peter WH, Kwan Tracy TC, Tam Kar Fai, Chan Karen KL, Young Phyllis MC, Lo Sue ST, et al. Beliefs about cervical cancer and human papillomavirus (HPV) and acceptability of HPV vaccination among Chinese women in Hong Kong. Prev Med 2007;45(2–3):130–4. [11] Vail-Smith K, White DM. Risk level, knowledge, and preventive behavior for human papillomaviruses among sexually active college women. J Am Coll Health 1992;40(March (5)):227–30. [12] Mays RM, Zimet GD, Winston Y, Kee R, Dickes J, Su L. Human papillomavirus, genital warts, Pap smears, and cervical cancer: knowledge and beliefs of adolescent and adult women. Health Care Women Int 2000;21(July–August (5)):361–74. [13] Dell DL, Chen H, Ahmad F, Stewart DE. Knowledge about human papillomavirus among adolescents. Obstet Gynecol 2000;96(November (5 Pt 1)): 653–6. [14] Marlow LA, Waller J, Wardle J. Public awareness that HPV is a risk factor for cervical cancer. Br J Cancer 2007;97(September (5)):691–4. [15] Pitts M, Clarke T. Human papillomavirus infections and risks of cervical cancer: what do women know? Health Educ Res 2002;17(December (6)): 706–14. [16] Tiro JA, Meissner HI, Kobrin S, Chollette V. What do women in the U.S. know about human papillomavirus and cervical cancer? Cancer Epidemiol Biomarkers Prev 2007;16(February (2)):288–94. [17] Pitts MK, Dyson SJ, Rosenthal DA, Garland SM. Knowledge and awareness of human papillomavirus (HPV): attitudes towards HPV vaccination among a representative sample of women in Victoria, Australia. Sex Health 2007;4(September (3)):177–80. [18] Dempsey AF, Davis MM. Overcoming barriers to adherence to HPV vaccination recommendations. Am J Manage Care 2006;12(December (17 Suppl.)): S484–91. [19] Brabin L, Roberts SA, Farzaneh F, Kitchener HC. Future acceptance of adolescent human papillomavirus vaccination: a survey of parental attitudes. Vaccine 2006;24(April (16)):3087–94. [20] Woodhall SC, Lehtinen M, Verho T, Huhtala H, Hokkanen M, Kosunen E. Anticipated acceptance of HPV vaccination at the baseline of implementation: a
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