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

Gui-Dn Tng, Gu-Qing Zeng, Bi-Xi Zho, Yun-Li Li, Rong Wng, Yn-Ping Wn,*

a Institute of Nursing, School of Nursing, University of South China, Hengyang, Hunan 421001, China

b Affiliated Nanhua Hospital, University of South China, Hengyang, Hunan 421001, China

Abstract: Objectives: To systematically review the knowledge attitudes and the influential factors on human papillomavirus (HPV) vaccination among Chinese women.Methods: Published studies on knowledge and attitudes of HPV vaccination for preventing cervical cancer among Chinese female population were retrieved using the major Chinese and English databases. Meanwhile, handwork retrieval was also conducted and the references including in the literature were retrieved. The quality of the literature was rigorously evaluated and extracted independently by two researchers and the data were analyzed and described by review manager 5.3 (RevMan5.3) software.Results: In all, 19 articles including 8 articles in Chinese and 11 in English were chosen. A total of 30,176 participants were included and the sample size ranged from 64 to 6,024. The overall awareness of HPV and HPV vaccine among Chinese women was at a low level. Chinese women generally showed poor knowledge about HPV and HPV vaccine. Acceptance of HPV vaccination among Chinese women was at a high level. Vaccination intentions were influenced by the theory of planned behavior (TPB) and measured by attitudes subjective norms and perceived behavioral control.Conclusions: The health authorities may evaluate and develop TPB-based interventions to increase HPV vaccination intentions of Chinese women. HPV vaccination programs should focus on carrying out multi-level and targeted health education and developing effective public health strategies after balancing the cost and benefit of HPV vaccine program. Medical staff should play the positive role in promoting the use of HPV vaccines in China. Integration of policy and community perspectives and multi-level interventions are essential to maximize the public health benefits of HPV vaccination.

Keywords: awareness · China · human papillomavirus · theory of planned behavior · vaccine · women

1. Introduction

Cervical cancer is the second most prevalent cancer and one of the top causes of cancer death worldwide among female.1It is estimated that 98.9 per 100,000 Chinese would be newly diagnosed and about 30.5 per 100,000 Chinese will die from cervical cancer in 2015.2Persistent human papillomavirus (HPV) infection is the primary factor of cervical cancer3,4and HPV vaccines have been recognized by World Health Organization (WHO) as the primary prevention to curb the potential disease process of cervical cancer. Because of the availability of HPV vaccines, cervical cancer has become preventable with the clear cause.5,6Three types of HPV vaccines have been developed. In 2016, the Cervarix was approved in China for use on female aims at preventing genital warts and cervical cancer. But few people know the relationship between HPV and cervical cancer and preventive effect of the vaccine, let alone understanding correctly. Studies have shown that the HPV vaccine will significantly reduce the burden of cervical cancer in combination with other preventive measures particularly.7

Theory of planned behavior (TPB) is one of the most influential theoretical models of behavioral research in social psychology. The TPB posits that attitude subjective norms and perceived behavioral control influence behavioral intention and subsequently behavior. Attitude refers to individual positive or negative appraisal of the behavior. Subjective norms refer to the social pressure that an individual perceives for a particular behavior. Perceived behavioral control refers to expecting obstacles to perform the behavior. Additionally, behavioral intentions directly determine behavior.

Therefore, this systematic review aimed to gain a better understanding of the cognition of HPV vaccine and use the TPB to analyze influential factors which are of great importance in identifying concerns and needs for formulating practical public health strategies for Chinese community.

2. Methods

2.1. Searching strategies

PubMed (Medline), Web of Science, CNKI, Wanfang Data, and CQVIP Data were searched by two researchers from December 2005 to December 2017. This vaccine (GardasilTM) 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.

2.2. Inclusion and exclusion criteria

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.

2.3. Data extraction and critical appraisal

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).

2.4 Data analysis

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

3. Results

As shown in Figure 1, 2,840 articles were identified after database searches, 39 were given full-text review with 19 meeting inclusion criteria.8-26

3.1. Study characteristics

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.8,9,11-26The 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

Table 1. Characteristics of included studies.

Table 2. (Continued).

Table 2. Extraction of study contents.

The majority of studies used random or cluster sampling methods.8,9,11-14,16,18-20,23-26Two studies in Taiwan, China used convenient sampling,15,17a study in Hong Kong, China used purposive sampling,10a study in Shanxi Province used systematic sampling,22while 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.

3.2. Awareness of HPV and HPV vaccine

Awareness of HPV was assessed by asking if the participants had heard of HPV in 18 studies.8,10,11,13-26The 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.21In Zhejiang Province, 39.1% of participants in urban areas and 27.1% of participants in rural areas had heard of HPV.19While the awareness rates of HPV were 8.0% among Uygur women and 19.0% among Han women in Xinjiang Uygur Autonomous Region.26Based on the findings of studies, in a rural area in Shanxi Province only 11.8% of women had heard of HPV,23which was far below the economically developed urban areas in China (46.9%).25Significant difference on the awareness of HPV was shown between urban and rural areas in China.

Figure 1. Selection of articles for inclusion in the systematic review after a search conducted in December 2017.

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.8,10,11,14,15,18,21,22,24,26More than half of participants in Hong Kong, China and Taiwan, China studies indicated that they had heard of HPV vaccine.10,14,15Only 5.5% of participants in Xinjiang Uygur Autonomous Region26had heard of HPV vaccine. The awareness of HPV vaccine was relatively lower in mainland China than those in Hong Kong, China and Taiwan, China.

3.3. TPB constructs

3.3.1. Attitudes

Most Chinese women had a positive attitude toward vaccination. A majority of studies reported individual HPV vaccine acceptability. Vaccination acceptance varied depending on the demographic characteristics of the participants but the rate of overall acceptance was high. In Gansu province, the rate of participants accepting HPV vaccination was 94.2%.20Six studies demonstrated great improvements on the acceptability of HPV vaccination after education intervention.10,11,13,19,20,22

Generally, most women showed strong willingness when they were reminded that HPV vaccine could prevent cervical cancer. Swarnapriya et al. reported that vaccine effectiveness was the most important attribute of vaccination.27In Beijing, 96.8% participants were willing to vaccinate because of its benefits.19In Taiwan, China, women with stronger beliefs of their susceptibility for cervical cancer and the disease severity were more likely to obtain the HPV vaccine.15

3.3.2. Subjective norms

Subjective norms were predominant factors in participants' intentions. Recommendations from significant others such as parents friends and healthcare providers influenced the Chinese women's decision to consider vaccination. In Taiwan, China, the greatest relation to intention was subjective norms which explained 60% of the variance in parental intention.17It was reported in four studies that the participants would more likely to receive the vaccine after recommendations from healthcare professional and hospital lectures.10,15,20,23In Shandong Province, most parents (81.0%) hoped HPV vaccine should be included in the expanded program immunization.8Similarly, women in both urban and rural areas believed that the government and healthcare organizations' recognition and attention were important.20,23

3.3.3. Perceived behavioral control

Cost was an important barrier for HPV vaccination. Some participants thought the vaccine should be free; while others indicated a minority willing to pay some amount although much less than the market price.8,19-26Parents were able to determine whether to endorse the HPV vaccine for their daughters. Mothers mainly worried that acceptance of the vaccine may be seen as an admission of risky or early sexual behavior by her daughter.9,18Young women worried that vaccination would give others the impression that they were sexually active.9,28A previous research in the Gaborone also revealed that participants were more likely to be vaccinated when they were involved in decision-making.29In addition, uncertainties on efficacy or safety of HPV vaccine was another important barrier for the uptakes of HPV vaccines. They worried about the potential side effects of HPV vaccine and duration of vaccine effectiveness.13,14,19,22,23The source of vaccine was also a concern. The majority of Chinese women indicated that they preferred vaccines provided by government or medical institutions.19,20

3.4. Other influential factors for acceptance of HPV vaccination

3.4.1. Parental education level and family income

Women with different educational levels had significant differences in awareness and vaccination willingness. The higher education they had the more they were willing to vaccinate. Participants' willingness with university and above qualifications was up to 74.4%.23Five studies reported significant association between family income and vaccine willingness. It was found that higher family income was a significant predictor of vaccine willingness.8,11,20,21,24

3.4.2. Sexual behavior

Among women whether or not they had sexual intercourse age of sexual onset number of sexual partners and preferred ways of contraception were important factors influencing HPV vaccination. Majority of the participants believed that sexually active women or women with multiple sexual partners should be vaccinated.10,15,17In Hong Kong, China, 86% of the participants agreed with vaccinating sexually active women.14Some participants believed that people with only one sexual partner had a low risk of getting infected with HPV and need not vaccinate.12The findings indicated that existing misconception on risk perception of cervical cancer was common among Chinese women.

3.4.3. Family history of gynecological tumors or infections

Family health history was related to women's willingness to receive the HPV vaccine. In Taiwan, China, the women with a personal or family history of gynecological tumors or infection were reported they had a high intention to vaccinate.15,17In mainland China, HPV vaccine for preventing HPV infection and sexually transmitted disease was the primary cause of vaccination. Of participants in Gansu Province, 73.6% women feared that they would suffer from cervical cancer if they had not vaccinated.23

4. Discussion

4.1. Knowledge and attitudes toward HPV vaccine

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.30Galbraith et al. found that African- Americans and Latinos' willingness to HPV vaccination were much lower than white Americans' willingness because of little knowledge.31The rate of awareness of HPV and vaccine in Italian teenagers was 92%.32The 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.33To 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.35In 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.33Utility 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.

4.2. Influential factors for acceptance of HPV vaccination

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.36This was consistent with Kester et al.37who 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.38Similar 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.39Women 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.40Physician's recommendation for HPV vaccination was significantly associated with vaccination among females in Louisiana and Alabama.41Those 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.42Thus, 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.43Young adults might be reluctant to receive the HPV vaccine because they were afraid of being labeled sexually active.28At 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.44Some 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.10,14,18,38,42The 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.45Health 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.8,9,13,14,19,20The 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 2008.46In 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.47A 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.48Together, 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.49It 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.

4.3. Limitations

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.19-26Only a study in Taiwan, China tested the ease of reading and clarity of self-administrated questionnaire prior to the survey.15Therefore, appropriate measures should be developed and the literacy level of participants should be assessed so as to obtain accurate data.

5. Conclusions

Cervical cancer is posing a big burden on Chinese women and can be preventable by the use of HPV vaccines. HPV vaccines were approved in 2016 and Chinese women have started to getting vaccinated. High HPV vaccination coverage is influenced by individual knowledge and attitudes. This review showed that the overall awareness and knowledge of Chinese women were very low. Raising the awareness and knowledge of Chinese women is extremely urgent. It must make an all-out effort to carry out multi-level and targeted health education but it should be careful to culturally sensitive people. Some major factors influenced the attitudes of HPV vaccination such as cost concerns on efficacy and safety of HPV vaccine recommendations from others and so on. The Health authorities may evaluate and develop TPB-based interventions to increase acceptance of Chinese women after considering all factors. Policymaker should seriously consider to developing effective public health strategies after balancing the cost and benefit of HPV vaccine program. It is necessary to expand the scope of medical insurance coverage and strengthen grass-roots healthcare project construction. Meanwhile, medical staffs should play a positive role in the recommendation of HPV vaccine. Together, all measures can maximize the public health benefits of HPV vaccination.

Acknowledgment

We would like to acknowledge the helpful comments provided by librarians.

Ethics approval

The study protocol was approved by the Ethics Committee of University of South China. Potential participants received information about the study and they were informed that their response will be considered an informed consent to participate in the survey. Consent for interviews was also obtained.

Conflicts of interest

All contributing authors declare no conflicts of interest.