Awareness and knowledge of human papillomavirus vaccination and their influential factors among Chinese women: a systematic review

PubMed (Medline), Web of Science, CNKI, Wanfang Data, and CQVIP Data were searched by two researchers from December 2005 to December 2017. This vaccine (Gardasil^TM) was approved by the FDA in 2006 for use in females aged 9–26 years. To increase the recall rate of literature we set the search time to December 2005. The search terms were “HPV” OR “Human papillomavirus” OR “HPV vaccine” OR “HPV vaccination” OR “cervical cancer vaccine” OR “cervical cancer prevention” AND “acceptance” OR “acceptability” OR “attitude” OR” awareness” OR “beliefs” OR “knowledge” OR “intention” OR “perception” OR “uptake” OR “willing” OR “willingness” AND “Chinese” OR “China” OR “Hong Kong” OR “Taiwan” OR “Taiwanese” OR “Macao” OR “Macau.” Meanwhile, manual retrieval was also conducted and the references including in the literature were retrieved.

Studies included in this review needed to meet the following criteria: (1) reporting awareness knowledge attitudes acceptances or beliefs toward HPV and HPV vaccine among Chinese female population; (2) studies that were primary researches collecting primary data and published in academic journals; and (3) studies published in either English or Chinese language.

Studies were excluded from this review if they meet the following criteria: (1) Chinese women were not included in sample population or specific results for Chinese women could not be extracted from the overall results; (2) studies that investigated the knowledge and attitudes of male healthcare professionals or students; (3) studies that focused on immunization efficacy or health technology assessment; and (4) reviews on recommendations and health practice guideline.

Data were extracted into a pre-specified data extraction form by one researcher and checked by another. Information about study design locations targeted sample research question key findings and interpretations was presented (data extraction shown in Tables 1 and 2).

No data were suitable for statistical pooling or meta-analysis because of the large clinical heterogeneity. Instead, the data were only analyzed by descriptive qualitative.

All articles were cross-sectional studies. Regarding study locations, 4 and 13 studies were conducted in Hong Kong, China and Mainland China, respectively. The rest two studies were from Taiwan, China. Eleven and eight articles were, respectively, published in English and Chinese. In all, 17 studies only used quantitative survey methodology.8, 9, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26 The rest used a qualitative–quantitative approach and conducted by focus group discussions. A supplementary questionnaire was administered to participants before and after group discussion to assess their knowledge attitudes and intention.10

The majority of studies used random or cluster sampling methods.8, 9, 11, 12, 13, 14, 16, 18, 19, 20, 23, 24, 25, 26 Two studies in Taiwan, China used convenient sampling,15, 17 a study in Hong Kong, China used purposive sampling,10 a study in Shanxi Province used systematic sampling,22 while another study did not mention the methods of conducting survey.21

There were 30,176 participants in this review and the sample sizes ranged from 64 to 6,024. The target participants of all studies were women. The age of the participant ranged from 13- to 71-years old and the most of the participants were above 18 years old.

Awareness of HPV was assessed by asking if the participants had heard of HPV in 18 studies.8, 10, 11, 13, 14, 15, 16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26 The overall awareness of HPV among Chinese women was at a low level. A study in Gansu Province, an area with high incidence of cervical cancer, showed that 94.3% of women had not heard of HPV and only 2.4% of women had known that HPV was linked to cervical cancer.21 In Zhejiang Province, 39.1% of participants in urban areas and 27.1% of participants in rural areas had heard of HPV.19 While the awareness rates of HPV were 8.0% among Uygur women and 19.0% among Han women in Xinjiang Uygur Autonomous Region.26 Based on the findings of studies, in a rural area in Shanxi Province only 11.8% of women had heard of HPV,23 which was far below the economically developed urban areas in China (46.9%).25 Significant difference on the awareness of HPV was shown between urban and rural areas in China.

Similarly, awareness of HPV vaccine was assessed by asking if the participants had heard of anti-cervical cancer vaccine or HPV vaccine in ten studies.8, 10, 11, 14, 15, 18, 21, 22, 24, 26 More than half of participants in Hong Kong, China and Taiwan, China studies indicated that they had heard of HPV vaccine.10, 14, 15 Only 5.5% of participants in Xinjiang Uygur Autonomous Region26 had heard of HPV vaccine. The awareness of HPV vaccine was relatively lower in mainland China than those in Hong Kong, China and Taiwan, China.

Previous studies on HPV vaccines were mainly concentrated in many Western and a number of Asian countries. However, studies on Chinese participants particularly were limited. Therefore, the purpose of this systematic review was to investigate the knowledge attitudes and the influential factors for HPV vaccination among Chinese women which was necessary for promotion and use of vaccines. Women’s knowledge and attitudes in China were influenced by different social demographic backgrounds. HPV vaccine has been licensed in Hong Kong, China and Taiwan, China since October 2006. It was a good news that Cervarix and Gardasil were approved in 2016 and 2017, respectively, in mainland China. The awareness of HPV vaccine was relatively lower in mainland China than those in Hong Kong, China and Taiwan, China because of less access to HPV vaccines.

Awareness of HPV and vaccines was one of the potential factors influencing the willingness to vaccinate.30 Galbraith et al. found that African-Americans and Latinos’ willingness to HPV vaccination were much lower than white Americans’ willingness because of little knowledge.31 The rate of awareness of HPV and vaccine in Italian teenagers was 92%.32 The government achieved high rate of vaccination uptake and completion depending on the integration between the public health and schooling systems which was up to 97.2% in Brazil.33 To raise public awareness and knowledge of HPV and vaccine were important indicators in preventing cervical cancer. However, previous studies indicated that Chinese women’s overall knowledge on HPV and HPV vaccine was poor. Most women failed to identify the relationship between HPV infection and cervical cancer and had many misconceptions concerning cervical cancer HPV and HPV vaccine. In contrast, an average of 50% women in Korea was able to identify correctly the link between HPV and cervical cancer.34

Despite lack of knowledge of HPV, the rate of acceptance of HPV vaccine among Chinese women was high. The results of low level of knowledge but high acceptance were similar to the outcomes of a study done in Haitian in 2014 when the HPV vaccine has just been approved.35 In fact, many participants had never been exposed to cervical cancer HPV and HPV vaccines before the survey. They may be difficult to make informed decisions about HPV vaccination so it is necessary to raise public awareness by further health education. The studies showed significant improvement in both level of knowledge and acceptance after education intervention; and these results were consistent with Western studies.33 Utility of information pamphlet and implementation of mass public health education on HPV vaccine are effective means for promotion and application of vaccination. For ethnic minorities, it should be considered that their mastery of Chinese Putonghua and the promotional materials are available in minority languages and Chinese Putonghua.

Studies showed parental educational level and family income were associated with awareness and willingness of HPV vaccine. Women with higher level of education may take the initiative to learn the relevant knowledge and had a higher level of acceptance to health knowledge and new things. So women with higher level of education may have a relatively higher acceptance. Vaccination willingness rates were much higher among women living in wealthier families than those among women living in poorer families. There was a positive correlation between vaccination rates and higher family income in the United States.36 This was consistent with Kester et al.37 who reported that vaccination coverage of young people in low-income families decreased significantly in the same year.

Being vulnerable to a health problem played a role in motivation for health behaviors.38 Similar to the findings from Taiwan, China, parental intention to daughters’ HPV vaccination was related to personal history of sexually transmitted diseases or family history of gynecologic tumors in Sweden.39 Women expressed a trust in vaccine recommendations from authorities and experts. If the HPV vaccine had been administered to adolescent girls during any healthcare visit in which they received another vaccine, the initiation rates for HPV vaccination in the United States would exceed 90% among this population.40 Physician’s recommendation for HPV vaccination was significantly associated with vaccination among females in Louisiana and Alabama.41 Those underlined the importance of healthcare professionals as key persons in spreading information about HPV and HPV vaccine. Although healthcare professionals had high level of awareness of HPV infection, they were lack of more comprehensive knowledge of HPV vaccine in mainland China.42 Thus, increasing HPV vaccination detailed knowledge and improving positive attitude of healthcare professionals are essential for enhancing the uptakes of HPV vaccines.

HPV vaccines were considered to prevent some sexually transmitted diseases by adolescents in the United States.43 Young adults might be reluctant to receive the HPV vaccine because they were afraid of being labeled sexually active.28 At the same time, Jumaan et al. found that focusing messages on cervical cancer protection rather than sexually transmitted diseases prevention appeared to help minimize sensitivities around girls’ sexuality.44 Some participants noted that those who frequently had sex or promiscuity needed vaccine and people who had only one sexual partner had a low risk of becoming infected with HPV.10, 14, 18, 38, 42 The most frequent reason for not accepting vaccination cited by mothers was ‘My daughter is too young to have sex’. Under the influence of traditional Chinese culture, sex has been a sensitive topic and sexually transmitted disease is a sexual stigma which is associated with immorality and infidelity. These findings were similar to the previous study in China that cultural issues such as modesty and embarrassment contributed to low cervical screening attendance.45 Health promotion should target at increasing women who have low perceived risk of HPV infection or a fear of social stigma. Public health services for Chinese women need to ensure that the philosophy of the staff and the approach used are culturally relevant especially for culturally sensitive women.

Suspicion of safety and efficacy of the vaccine were reported in some studies as the primary reason for refusing vaccination. Participants concerns about the possibility of lasting health problems.8, 9, 13, 14, 19, 20 The study in the USA comparing parental responses over time found that more cited safety concerns as a reason for not vaccinating their adolescents in 2010 than that in 2008.46 In fact, many clinical trials demonstrated that HPV vaccines had a promising effectiveness against cervical cancer and the risk of adverse events related to vaccination were acceptable. The vaccines have been already licensed in many countries.47 A survey in Japan showed that a hypothetical restart of a governmental recommendation for the vaccine would induce 4.1% of all the mothers who were more likely to encourage their daughters to get vaccinated without any other preconditions.48 Together, health authorities and mainstream media should spread the impartial and accurate messages to the public and guarantee the safety of HPV vaccines. If possible, the vaccines should be supplied through government programs. It is rise to make medical staff play the positive role in promoting the use of HPV vaccines.

The cost presented a significant barrier to implementation in China. It was found that more than 50% participants could not afford the HPV vaccines and wanted the government to pay all or part of the costs. A huge gap between affordable price and actual price inevitably leaded to a decline in vaccination rates. We can learn from the Global Alliance for Vaccines and Immunization (GAVI) policy in low- and middle-income countries which made a great success.49 It can be considered that cost is shared among recipients government public health insurance companies charities international health organization and pharmaceutical companies. To lower the price of HPV vaccine to an acceptable level, the integration of an appropriately expanded coverage of health insurance and a reasonable cost-sharing mechanism should be conducted.

In 18 studies on knowledge and acceptance of HPV and HPV vaccine, the results were inconsistent. Study designs, sample sizes, sampling techniques, sociodemographic characteristics of population measures, and locations may result in the low comparability. Owing to disparities in wealth and unequal development among cities, the results may not accurately represent the knowledge and attitudes of Chinese women in general. Most studies used convenience sampling methods so that samples were not representative. Altogether, sampling among different geographic regions should be stratified based on population density and development in future researches. The assessment and outcome measures differed greatly across the studies and comparability was limited. All studies used a self-administered questionnaire and seven articles did not report the source of measures or questionnaires.19, 20, 21, 22, 23, 24, 25, 26 Only a study in Taiwan, China tested the ease of reading and clarity of self-administrated questionnaire prior to the survey.15 Therefore, appropriate measures should be developed and the literacy level of participants should be assessed so as to obtain accurate data.