Knowledge and Practices Regarding Human Papillomavirus and Cervical Cancer Screening Among Women in Low-Income Areas of China: A Cross-Sectional Study

Background: Persistent human papillomavirus (HPV) infection is the primary cause of cervical cancer. However, this can be prevented through vaccination and screening. This study aimed to clarify the relationship between behavior, knowledge, and attitude toward cervical cancer and regular screening and HPV infection among women in Lueyang County. Methods: Women who underwent cervical cancer screening at the outpatient department of a maternal and child health center between September and December 2021 were invited to participate. In total, 2,303 women completed the questionnaire. Women who underwent regular or irregular screening were 1:1 matched for age. Differences in knowledge of HPV and attitudes toward HPV vaccination among different populations were assessed. Logistic regression analysis was performed to identify the factors influencing HPV infection. Results: In total, 417 pairs of women who underwent regular and irregular screening were successfully matched. Multivariate logistic regression results indicated that age is a risk factor for HPV infection (OR=1.056 95%CI: [1.031 1.082]), while regular screening acts as a protective factor against HPV infection (OR=0.174 95%CI: [0.117 0.259]). Additionally, regular screening was associated with a higher level of knowledge about HPV among women compared to those who did not undergo regular screening (p<0.001). Conclusions: Women in Lueyang County have low levels of knowledge regarding HPV and cervical cancer. Regular screening is a protective factor against HPV infection. The regular screening group demonstrates a higher level of HPV knowledge compared with the irregular screening group. These findings highlight the importance of regular screening and the need to strengthen public health education.


Introduction
Cervical cancer is the only cancer with a definitive cause attributed to persistent infection by high-risk human papillomavirus (HPV) [1].Therefore, further exploration in this field is warranted in future research to bolster HPV vaccination, regular screening, and other efficacious measures aimed at reducing the incidence and mortality of cervical cancer, as evidenced in developed nations [2,3].Thus, in 2009, under the auspices of the All-China Women's Federation and the Ministry of Health, China launched a screening program for "two cancers" (cervical and breast cancers) and implemented free cervical cancer screening for rural women aged 35-64 years [4].However, despite the widespread recognition of cervical cancer screening, it has low participation rates, especially in rural and western regions, compared with eastern regions.The disparity in participation rates across various socioeconomic and geographic provinces poses a significant challenge in preventing cervical cancer [5].Currently, China's cervical cancer screening rate is far below the target of the World Health Organization of 70% screening coverage [6].
Multiple elements impact women's engagement in cervical cancer screening, encompassing age, educational attainment, socioeconomic standing, and awareness of cervical cancer [7].Previous studies have demonstrated a significant correlation between cervical cancer knowledge and the rate of screening participation [8,9].An insufficient understanding of cervical cancer is considered one of the most important factors affecting participation rates [10].That is, women who have participated in screening generally have greater knowledge of cervical cancer than those who have not undergone screening [11].
Lueyang County, which has high cervical cancer incidence and mortality rates, is a low-income region in China [12].With an average educational level below the national standard, most of the residents live as farmers or migrant workers.Despite the initiation of annual cancer screenings in 2017, orchestrated by the local maternal and child health centers in collaboration with regional health centers and village doctors, the uptake in Lueyang County remains low.A limited number of women benefit from free screening, whereas several abstain from participation, which is potentially attributable to insufficient health awareness, financial constraints, and logistic complications [13].
This study aimed to examine the correlation between cervical cancer knowledge and adherence to regular screening practices.Additionally, we aimed to evaluate the effectiveness of regular screening for early detection of cervical cancer.Moreover, the present study aimed to understand women's attitudes toward cervical cancer prevention in high-risk areas.The primary objective was to increase the adoption of regular cervical cancer screening by developing evidence-based health education strategies aimed at enhancing understanding of cervical cancer and, consequently, its prevention.

Study design and ethical considerations
This study used a cross-sectional design and was conducted at Lueyang County Maternal and Child Health Hospital in Hanzhong City, Shaanxi Province.We collected information from women who underwent cervical cancer screening and invited them to complete our questionnaire.The content of our questionnaire was derived from a literature review and expert consultation.After obtaining informed consent from the participants, professional nurses provided guidance on completing the questionnaire.This study was approved by the Ethics Committee of Lueyang County Maternal and Child Health Hospital (Approval number: 2021-001).

Data collection and inclusion criteria
We invited all women who underwent cervical cancer screening from September to December 2021 to complete a paper-based questionnaire, and the completed questionnaires were subsequently entered into a data platform by professional personnel.Additionally, we registered the HPV test results of all patients on the data platform.Women from Lueyang County aged 20 or more and agreed to participate in the survey were included.Women with mental illnesses, depression, and a history of cervical cancer were excluded.Ultimately, 2,303 women participated in our study.

Questionnaire
The questionnaire included demographic information, health-related knowledge about HPV, regular participation in cervical cancer screening, and attitudes toward HPV vaccination.We defined women who had been screened for cervical cancer in the last 3 years as regularly screened and women who had not been screened for cervical cancer in the last 3 years as not regularly screened.
Notably, there are a total of seven questions of HPV health-related knowledge, the first question is "Do you know about HPV?",Only if the answer is "YES" can you continue to answer the next six questions.The next six questions are "HPV is an important etiological factor of cervical cancer" "HPV can cause genital warts in both men and women" and "HPV can be transmitted through sexual contact" "Most HPV infections can naturally regress without treatment" "Men can also be infected with HPV" "Condoms can prevent HPV infection" Participants answered "Know" or "Unknown" based on their perceptions.
Attitude refers to the willingness to receive the HPV vaccine, with a positive attitude indicating willingness to receive the HPV vaccine and a negative attitude indicating unwillingness to receive the HPV vaccine.
Although no formal validation of this questionnaire was performed, we performed quality controls, professional nurses training, and extensive reviews throughout the entire study.This included standardized training for all surveyors prior to the commencement of the official survey to ensure that they fully understood the research content and questionnaire items and to unify operational standards.During the survey, surveyors checked the completeness of the questionnaire responses and reminded participants to fill in any missing items.Post-survey, the validity of the questionnaires was reviewed to exclude invalid responses, and finally, data from the questionnaires were entered using a dual-entry system.

Statistical analysis
For descriptive analysis, SAS version 9.4 was employed, while SPSS was utilized for participant matching.Participant demographic and clinical characteristics were summarized, with continuous variables presented as mean±standard deviation and categorical variables as proportions (%).Significant associations in contingency tables were tested using standard Pearson's chi-squared test.If the P-value calculated in these analyses was <0.05, the difference was considered significant.We aimed to analyze the differences in HPV knowledge between the regular and irregular screening groups.To increase the effects of reducing confounding factors and enhance the comparability of the regular and irregular screening groups, we established the regular and irregular screening groups using age as a matching variable, with 1:1 matching.Additionally, multivariate logistic regression was used to assess the influencing factors of HPV infection.
This article was previously posted to the medRxiv preprint server on November 16, 2023.

Results
In total, 2,303 women participated in this study, 419 (mean age, 47.54±8.48years) in the regular screening group and 1,884 (mean age, 49.26±8.45years) in the irregular screening group.Out of the participants, a total of 465 participants tested positive for HPV.A total of 39.67% and 51.98% of women in the regular and irregular screening groups, respectively, were farmers.In the regular and irregular screening groups, 195 (47.33%) and 816 (43.54%) women, respectively, had secondary education (middle/high school).Furthermore, a greater proportion of women in the regular screening group had a university education than those in the irregular screening group.In the regular screening group, 56.12% of the women had an annual household income ranging from RMB 10,000 to 30,000.Notably, 2.94% and 0.86% of the women in the regular and irregular screening groups, respectively, received HPV immunization.A comprehensive summary of the participants' characteristics is provided in Table

TABLE 3: HPV awareness and regular screening among 2303 participants
To enhance the comparability between the two groups, we paired them according to age, resulting in 417 matched pairs with an equal number of participants in both groups after matching(Table 1).After matching, the two groups were of equal age.Compared with the irregular screening group, the regular screening group was more educated and had a higher annual household income (P<0.05).There were 216 (51.80%) positive HPV test results in irregular screening and 84 (20.14%) in regular screening, (p<0.001).After matching, 165 (39.95%) and 191 (46.59%) women in the regular screening group and irregular screening group were farmers by occupation, respectively (p=0.045).Overall, the educational level of women in the matched regular screening group was higher than that of irregularly screened women.The number of regular gynecological check-ups was also higher in the regular plus cervical cancer screening group 362 (86.81%) than in the irregular screening group (p<0.001).
Table 4 shows the differences in HPV knowledge between the regular and irregular screening groups.
Regarding the question "Do you know about HPV?" the number of individuals with HPV knowledge in the regular screening group (214 [51.32%]) was higher than that in the irregular screening group (107 [25.66%]) (P<0.0001).Among the participants with HPV knowledge, no significant difference was found between the regular and irregular screening groups in terms of HPV-related diseases and transmission, prognosis, and prevention of HPV infection.

TABLE 5: Attitudes toward HPV vaccine among the regular screening group and the irregular screening group
A total of 295 women provided reasons for not undergoing regular screening.Multiple reasons could be simultaneously selected."Do not know how to check regularly" was the most frequently selected reason, followed by "Do not know the significance of screening."The third reason was "No symptoms," and a small percentage of reasons included feeling unnecessary and having no time.Figure 1 shows the reasons for not having regular screening.

FIGURE 1: Reasons for not having regular screening Discussion
This study mainly comprised women in underdeveloped areas, with the objective of assessing the patterns of regular screening behavior and the level of awareness regarding cervical cancer among this specific demographic.Our study demonstrated that women who were regularly screened were less likely to be infected with HPV than those who were irregularly screened, which suggests the importance of regular screening.Moreover, awareness of cervical cancer was higher in the regular screening group than in the irregular screening group.These results provide a basis for the development of grassroots public health work emphasizing the importance of cervical cancer screening and health education.This is particularly crucial in low-income areas where targeted efforts can significantly contribute to improving healthcare outcomes.
In our study, the percentage of women screened in the past 3 years was 18.01%, which is markedly lower than the regular screening rate among women in urban areas (82.14%), according to a previous study [14].In 2009, China launched the National Cervical Cancer Screening Program for Rural Areas, providing complimentary cervical cancer screening to registered rural women aged 35-64 years.Over the last 10 years, the rates of cervical cancer screening have risen in both urban and rural regions of China [15].However, these rates still fall below the WHO target of achieving 70% coverage for cervical cancer screening.Furthermore, disparities persist, revealing inequalities in screening rates between urban and rural areas and between the eastern and western regions of the country [13].Factors such as inadequate or low income, elevated costs associated with attending screening (including transportation constraints and time commitments), and the absence of free employee check-ups, can contribute to reduced willingness to undergo screening for cervical cancer [5].Screening rates tend to be lower in older than in younger women.Specifically, women aged >50 years exhibit significantly lower screening rates than those in the 35-49-year age group, as indicated in a previous study [16].Our own study corroborates these findings, revealing that women in the regular screening group were generally younger than those in the irregular screening group.This phenomenon can be attributed to lower awareness of cervical cancer and entrenched traditional beliefs among older women [17].
Another significant factor contributing to low rates of cervical cancer screening is the limited awareness of screening, which poses a common barrier, especially in low-and middle-income countries.Several studies have consistently shown a positive correlation between cognitive awareness and the willingness to participate in screening [18,19].This aligns with findings from cervical cancer awareness surveys conducted in various regions [20,21].In line with these observations, our study also indicates that women in this economically disadvantaged area possess low knowledge about cervical cancer.A common belief among women is that screening is unnecessary if they are not experiencing symptoms [22].This lack of awareness regarding the early features and risk factors for cervical cancer can result in patients with early stage cervical cancer missing an optimal window for treatment.Therefore, it is crucial to enhance awareness among women to promote screening and ensure timely intervention.
Health education is an effective method for raising awareness about cervical cancer.Providing education to women through lectures and video dissemination results in a substantial increase in their willingness to undergo cervical cancer screening.In Abera's study, the intervention group demonstrated a remarkable and sustained increase of 46.4% in screening willingness during subsequent follow-up visits.This underscores the importance of health education in fostering women's participation in screening initiatives [23][24][25].Nevertheless, notably, women in underdeveloped areas, particularly older women, may not have received systematic education, face challenges in reading and writing, or may have limited access to useful information via mobile phones.Additionally, owing to their geographical distance, they may encounter difficulties in accessing public health services.Undertaking health education initiatives for this demographic poses a significant challenge given these factors.Addressing these challenges requires innovative and targeted approaches to ensure the effective communication and education of women in underdeveloped areas.
HPV vaccination is considered the primary preventive measure against cervical cancer [26].Observations in Italy and Norway among women who have received the vaccine indicate a decrease in HPV disease incidence rates, underscoring the necessity and effectiveness of the vaccine [27,28].However, in China, only a few cities with a high socioeconomic status have implemented free HPV vaccination programs [29].In our study, although women who were not screened regularly exhibited lower socioeconomic status and awareness of HPV compared to those who underwent regular screenings, they still demonstrated a comparable willingness to accept HPV vaccination.This may be attributed to the high costs associated with HPV vaccination, difficulties in scheduling appointments, and a lack of supportive policies, which hindered their uptake [30].
The Lueyang County government recently devised a plan to implement a flat-rate subsidy for the cost of preventive HPV vaccination for girls aged 9-14 years within the county.This initiative aims to encourage HPV vaccination among girls of appropriate age and increase the local vaccination rate.However, notably, the vaccine has a limited timeframe and does not encompass all HPV strains.Even with vaccination, regular cervical cancer screening is essential for comprehensive prevention.The integration of vaccination and screening is crucial for the effective implementation of primary and secondary prevention measures against cervical cancer.
Limitations: This study has some limitations.First, our study specifically targeted women in less-developed regions to provide evidence of the importance of regular screening in economically disadvantaged areas.It is not intended for extrapolation to regions with higher economic levels and does not claim national applicability.Second, this was a cross-sectional study, and prospective observational studies are required to obtain long-term outcomes in regularly and irregularly screened women.Third, although we identified an association between screening behavior and awareness, a causal relationship was not established.This underscores the need for further studies to provide evidence-based insights into subsequent cervical cancer prevention and management in Lueyang County.Continued investigation will enhance our understanding of the factors influencing screening behavior and aid in the development of more targeted and effective preventive strategies.

Table 2
shows that age was a risk factor for HPV infection (odds ratio [OR]=1.056,95% confidence interval [CI]: 1.031-1.082).In contrast, regular screening was a protective factor for HPV infection (OR=0.174,95% CI: 0.117-0.259),suggesting that individuals who undergo regular screening have a lower likelihood of infection with HPV compared with those who do not.

TABLE 4 : Knowledge of HPV between the regular screening group and the irregular screening group
*The number of respondents who answered "YES" to the "Do you know about HPV?" question.

Table 5
shows attitudes toward the HPV vaccine among the regular screening group and the irregular screening group.In the regular screening group, 237 (56.83%) individuals were aware that "HPV infection can be prevented by vaccination," whereas in the irregular screening group, 194 (46.52%) individuals had this knowledge (P=0.0029).Regarding "willingness to receive HPV vaccination," most of the participants in both the regular (348 [83.45%]) and irregular (345 [82.73%]) screening groups demonstrated a positive attitude toward HPV.Regarding the willingness to have their daughters vaccinated against HPV, mothers in the irregular screening group (17 [6.97%]) exhibited a higher level of hesitancy compared with mothers in the regular screening group (4 [1.70%], P=0.004).
Reasons you don't want to get the HPV vaccineThere are no risk for cervical cancer It doesn't make any difference if you're inoculated or not.The HPV vaccine is not yet widely available Inoculation can have varying degrees of side effects Distrust in the source of HPV vaccine Unable to afford vaccination 2.2.Reasons why you would like to receive the HPV vaccine Considered to be of benefit You can get cervical cancer if you don't get vaccinated You can get HPV if you don't get vaccinated You can get genital warts if you don't get inoculated.If you have a daughter would you want your daughter to get the HPV vaccine?Reasons why you don't want your daughter to get the HPV vaccine Doubts about the safety and efficacy of vaccines Mistrust of the source of HPV 2024 Chen et al.Cureus 16(3): e55930.DOI 10.7759/cureus.55930