Cervical cancer, the human papillomavirus vaccine, and cervical screenings from 2004—2021: a Google Trends analysis in Japan

DOI: https://doi.org/10.21203/rs.3.rs-1710203/v1

Abstract

Background

The World Health Organization (WHO) established a global strategy to accelerate the elimination of cervical cancer in 2020; fortunately, it can be effectively controlled or prevented by the human papillomavirus (HPV) vaccine. Nevertheless, Japan has been experiencing an HPV vaccine crisis since 2013, with a vaccination rate of less than 1% lasting for seven years. We examined trend changes related to cervical cancer topics and assessed the feasibility and limitations of Google Trends as an indicator of public health surveillance.

Methods

We collected search query data from Google Trends and the annual number of cervical cancer cases from the National Cancer Center, Japan. We then conducted a chronological and geographical analysis of the public interest in the phrases “cervical cancer,” “HPV vaccine,” and “cervical screening” from 2004—2021. We calculated correlations between the annual number of cervical cancer cases and the search terms. We also detected change points in public search interest. Finally, we analyzed subregional-level search interest disparities.

Results

Japanese public search interest in “cervical cancer,” “HPV vaccine,” and “cervical screening” increased from 2010—2013. Subsequently, interest in “cervical cancer” and “cervical screening” remained stable and relatively high, while interest in “HPV vaccine” was suddenly minimal. The actual number of cervical cancer cases showed a strong correlation with search volumes for “cervical screening” (r = 0.953, p < .001) and “cervical cancer” (r = 0.898, p < .001), respectively. In 2020, the public reignited its interest in “HPV vaccine.” We detected six change points in these three topics around 2010, 2013, and 2020, which aligned with critical policy decisions. Prefectures’ public interest levels were different for these three topics.

Conclusions

The Japanese public retained low interest in “HPV vaccine” from 2013—2020, while interest in “cervical cancer” and “cervical screening” terms was relatively high. Encouragingly, the public reignited its interest in “HPV vaccine” in 2020, which is expected to promote vaccination. Google Trends can extend unique perspectives for authorities to understand public concerns nearly synchronously, but it has a limited interpretation in subregions.

Background

Cervical cancer is one of the most common cancers and the leading cause of cancer-related mortality in women worldwide, despite being a preventable illness. Between 2018 and 2030, the annual number of cervical cancer cases is projected to rise from 570 000 to 700 000, with 311 000 to 400 000 eventual deaths worldwide. To avoid unnecessary fatalities, the World Health Organization (WHO) has developed a global strategy for accelerating cervical cancer elimination by 2030 [1]. Many countries are making efforts to introduce and scale up HPV vaccination, ensuring that 90% of girls aged at least 15-years-old are fully vaccinated by 2030. As of December 2021, 116 countries have included the human papillomavirus (HPV) vaccine in their national immunization programs. Norway, Mexico, Rwanda, and other countries have demonstrated that 90% coverage is attainable [2]. However, Japan is undergoing an HPV vaccine crisis, which began in 2013 and lasted for seven years, with vaccination coverage ranging from approximately 70%, to less than 1% [3].

Japan approved the HPV vaccine in 2009 and began subsidizing it publicly in 2010 [3]. The HPV vaccine was included in the national routine immunization schedule for girls aged 12—16 in April 2013. As HPV vaccination became widespread in Japan, the mass media reported unverified side effects among recipients. In response to these reports, the Ministry of Health, Labour and Welfare (MHLW) withdrew the proactive recommendation for HPV vaccination in June 2013, regardless of insufficient scientific evidence linking vaccination to adverse events. Municipalities subsequently curtailed the dissemination of HPV vaccination information among targeted users. In 2018, only 97 of 1741 reporting municipalities targeted adolescent girls about the importance of HPV vaccination [4]. As a result, Japan's vaccination confidence was reported to be among the lowest worldwide in 2020 [5]. HPV infection is the only vaccine-preventable disease (VPD) with more than 100 000 disability-adjusted life years (DALYs, a measure of overall disease burden, expressed as the number of years lost due to ill-health, disability, or early death) experienced annually from 2008—2020 [6]. Based on real-world evidence, infection rates have risen once again [7], representing a critical public health problem in Japan.

Vaccine hesitancy is a stumbling block in the promotion of vaccination. It was named by the WHO as one of ten global health threats in 2019 [8] and defined as a “delay in acceptance or refusal of vaccines despite availability of vaccine services [9].” Individuals who hesitate to receive vaccination may have multiple concerns about efficacy and safety, which may be impacted by others' decisions to postpone or reject vaccination [10]. Although the Ministry of Health, Labour and Welfare (MHLW) officially announced a proactive recommendation for the HPV vaccine on Nov 26, 2021, there is still a long way to go toward achieving sufficient public acceptance. Enhancing the understanding of public attitudes toward cervical cancer and HPV vaccines is critical for developing tailored educational programs and improving HPV vaccination rates. Previous studies have examined the present scientific evidence, the MHLW's poor risk management and communication, troubles with mass media reporting, and assessments of the HPV health burden in Japan [1113]. To the best of our knowledge, no studies have addressed public concerns about cervical cancer by searching for interest and health information-seeking behavior.

Google Trends is an online tool for assessing data derived from public internet searches, which provides unique insights into public attitudes toward cervical cancer in Japan. Google Trends is available for discovering search queries from various countries and their sub-regions. Unlike traditional public health surveillance, which takes years to gather data based on government implementation [14], Google Trends automatically collects real-time data and generates quantitative and qualitative information, which can be used for informatics research on communicable and non-communicable diseases [15, 16]. Google Trends can enhance traditional public health surveillance and assist professionals with better awareness of public reactions and sentiments regarding diseases [17—19]. Additionally, Google Trends can identify unmet health information needs [18]. Internet search query data are valuable for cervical cancer prevention and control; however, no relevant study has yet explored this issue in Japan.

Hence, we aimed to examine search trend changes around cervical cancer and assess the feasibility of Google Trends as an indicator of public health surveillance as well as its limitations. This study conducted chronological and geographical analyses of the search terms “cervical cancer,” “HPV vaccine,” and “cervical screening” to understand public concerns and extend real-world evidence on public interest and health information-seeking behaviors. In addition, the disparity of public search interests in subregions may help municipalities develop tailored strategies for health promotion.

Methods

Data

We collected search query data from Google Trends [20] and cervical cancer case information from the National Cancer Center, Japan (NCCJ) [21]. Google Trends offers relative search volumes (RSVs) to illustrate the popularity of a particular search topic or term in a precise geographic location over a specified period. RSV is a value ranging from 0—100, where 0 indicates that there is insufficient data for this term, and 100 indicates the term's peak popularity [14, 22].

HPV vaccination has been proven safe and effective in clinical trials and post-marketing surveillance for prevention of HPV infections, high-grade precancerous lesions, and invasive cancers [23]. However, HPV vaccination cannot replace cervical cancer screenings. Cervical screening programs are necessary to detect and treat precancerous lesions and cancers to reduce morbidity and mortality. Hence, we selected “cervical cancer,” “HPV vaccine,” and “cervical screening” as search topics, restricting the region to Japan and inclusive of all search categories. The plus sign (+) in Google Trends has the function of “OR” and can be used to connect multiple terms to form a broad phrase [24]. Table 1 lists the topics and search terms used in our study. Japanese RSV data between January 1, 2004, and December 31, 2021, were collected and exported into CSV files. In addition, we gathered RSV data by sub-region in Japan during the same period for geographical analysis. We downloaded the polygon shapefile containing the first-level administrative divisions of Japan from the Stanford Digital Repository [25].

Table 1

Query topics and search terms

Query topic

Search terms (Japanese)

Cervical cancer

“子宮頸がん,” “子宮頚癌,” “子宮頸ガン,” “HPVがん,” “HPV癌,” and “HPVガン”

HPV vaccine

“HPVワクチン,” “子宮頸がんワクチン,” “子宮頸癌ワクチン,” and “子宮頸ガンワクチン”

Cervical screening

“子宮頚がん検査,” “子宮頚癌検査,” 子宮頚ガン検査,” “子宮頚がん検診,” “子宮頚癌検診”and “子宮頚ガン検診”

Statistical Analysis

To compare information-seeking behavior and cervical cancer incidence, we calculated the Pearson correlation coefficient (r) for significance [26] between each query topic’s annual RSV and the annual number of cancer cases. As the NCCJ's annual number of cervical cancer cases was only up to date as of 2018, the correlation was subsequently restricted from 2004—2018. Furthermore, in order to observe the trends of long-term public interest in each topic, we used the pruned exact linear time (PELT) algorithm [27] by Ruptures [28] to detect change points without knowing the number of breakpoints in advance. Monthly RSV data for each query topic were used for change detection analysis between January 2004 and December 2021. For the geographical analysis, we shaped the geographical map using GeoPandas [29] for each topic from 2004—2021. Various prefectures in Japan are depicted as color-coded heatmaps, based on RSV indices. We annotated prefectures in the heatmaps which had RSV indices > 90 as well as the bottom five.

Results

As shown in Figure 1, the overall RSV of the term “cervical cancer” increased between 2009 and 2013, while the RSV of “HPV vaccine” decreased from 2013—2020. After that, the RSV of “HPV vaccine” and “cervical cancer” surged, coinciding with the MHLW’s official announcement to resume proactive recommendations of the HPV vaccine on November 26, 2021, which had been previously suspended since June 2013 [30]. The RSV value for “cervical screening” increased from 2012 until 2021. Compared with “HPV vaccine” and “cervical screening,” the RSV for “cervical cancer” maintained a high value of approximately 50. The actual annual number of cancer cases was coincident with the change in RSV value of “cervical cancer” (r=0.898, p<.001) and “cervical screening” (r=0.953, p<.001), indicating that an increase in the number of cancer cases may lead to a higher public interest in information regarding “cervical cancer” and “cervical screenings” over time. “HPV vaccine” RSV did not have strong correlations (r=0.454, p<.001) with the annual number of cervical cancer cases. As shown in Figure 2, in the sum of these three topics, RSV values displayed three distinct peaks in 2010, 2013, and 2021. Public search interest dovetailed with the launch times of the authorities' policy and mass media reports.

In Figure 3, we show six change points detected by the PELT algorithm that represent long-term trends, including two change points around 2010, three around 2013, and one change point around 2020. The MHLW claimed that the HPV vaccine was a routine program in 2010, but the mass media subsequently reported adverse effects. From 2010—2013, public search interest fluctuated dramatically until the MHLW withdrew proactive recommendations for the HPV vaccine. No subsequent change points emerged from public attention between 2013 and 2020. As of 2020, the public has reignited its interest in the HPV vaccine. The MHLW revisited the safety of the HPV vaccine and resumed proactive recommendations in November 2021. Professional institutions and social organizations played a positive role with their involvement in this campaign. However, in 2021, no change points were detected with “cervical cancer” or “cervical screening” topics, indicating that resumptive proactive recommendations did not immediately excite public interest. 

Figures 4 and 5 show the geographical maps containing public interest in “cervical cancer,” “HPV vaccine,” and “cervical screening” by prefecture. We labeled prefectures with >90 indices in English and Japanese and the bottom five. In Figure 4, the Hokkaido, Fukuoka, and Osaka prefectures presented more public interest in “cervical cancer,” while the Kyoto, Okayama, Kumamoto, Tokushima, Nara, and Yamanashi prefectures focused on “HPV vaccine.” Hokkaido, Saitama, Kagoshima, and Osaka prefectures also enquired about “cervical screening.” In Figure 5, the Aichi, Saga, and Okinawa prefectures demonstrated relatively less interest for “HPV vaccine,” while the Kyoto, Shizuoka, and Tottori prefectures exhibited less concern for “cervical screening.” Municipalities should promote relevant information dissemination on cervical cancer-related health education. Appendix 1 presents the original data.

Discussion

In this study, we used Google Trends data to conduct a chronological and geographical analysis of specific HPV terms to understand relative public concern. Overall Japanese public search interest in “cervical cancer,” “HPV vaccine,” and “cervical screening” phrases increased between 2010 and 2013. Subsequently, interest in “cervical cancer” and “cervical screenings” remains stable while “HPV vaccine” decreased in volume. In 2020, the public reignited its interest in “HPV vaccine” rather than “cervical cancer” or “cervical screening.” In relation to the actual annual number of cervical cancer cases, the search interest in “cervical cancer” and “cervical screening” showed a strong correlation, but “HPV vaccine” did not. Our results provide quantitative evidence that public interest coincides with government policy by change points detected around 2010, 2013, and 2020. Prefectures exhibited different search interests for these topics. We examined the chronological changes and geographical differences in cervical cancer and its related terms using public search engine interest. We believe that Google Trends can provide a unique perspective for policymakers and professionals alike.

Japan has been experiencing an HPV vaccine crisis that started in 2013 with a rapid decline in vaccination rates. When correspondingly low coverage of vaccination rates was < 1%, public search interest in “HPV vaccine” also maintained a low search volume. From 2013 until 2020, the MHLW suspended its proactive HPV vaccine recommendation campaign. Positive articles became less frequent than negative articles, following negative impacts from mass media reporting [12], which negatively affected Japanese mothers’ intentions to vaccinate their adolescent daughters [31]. The WHO also commented that this policy decision based on weak evidence led to a lack of vaccine administrations, resulting in real harm [32]. Subsequently, evidence has shown that HPV infection rates rose again [7], which resulted in a persistently high burden of disease, despite being preventable [6].

Fortunately, the MHLW announced a proactive recommendation for HPV vaccination again in 2021. From our findings, this policy reignited the public interest. We expect this nationwide HPV vaccine reintroduction to better control cervical cancer, achieving the target set by the WHO for a 90% coverage rate for girls by 2030 [33]. In contrast, search interest in “cervical cancer” and “cervical screening” maintained a stable and relatively high volume and was strongly correlated with the number of actual cancer cases. However, interest volumes of “cervical screening” are far less than for “cervical cancer.” In real-world situations, women receive a low percentage of cervical cancer screenings, despite the increase in cancer prevalence [34]. Only 22.2% of women in their 20s underwent cervical cancer screenings in Japan, this is comparatively low to other developed nations [35].

From 2013—2021, we detected three critical time points (2010, 2013, and 2020) for public interest in cervical cancer. In 2009, the HPV vaccine was licensed and it was publicly subsidized in 2010. In 2013, the MHLW withdrew their proactive recommendation for the HPV vaccine, due to sensationalized media reports of adverse events. In 2020 and 2021, several vote campaigns related to the HPV vaccine were organized by Change Japan, which is an online signature site used by 400 million people worldwide [36]. The campaign “Call for the resumption of proactive HPV vaccination recommendations” was lunched on August 27, 2021 and endorsed by 58222 people. In addition, the MHLW revisited the safety of the HPV vaccine and resumed its recommendation. In 2017, the Japan Expert Council on Promotion of Vaccination, a body of 17 academic societies from a broad range of fields, sought a strong endorsement for HPV vaccination [37]. In 2019, the Liberal Democratic Party (LDP) in Japan took up this challenge and launched a parliamentary league to actively promote HPV vaccination recommendations [38]. However, the public did not show increased interest in “cervical cancer” in 2017 or 2019, as search interest trends did not change. Effective information dissemination has been proven to promote public health. Authorities can refer to search data to understand the local public response to events in real-time and facilitate rapid adjustment of promotional strategies.

Geographical search volumes for “cervical cancer,” “HPV vaccines,” and “cervical screening” showed disparities. Hokkaido and Osaka prefectures showed more public interest in “cervical cancer” and “cervical screening,” but not in “HPV vaccine.” Kyoto, Okayama, Kumamoto, Tokushima, Nara, and Yamanashi prefectures were more interested in “HPV vaccine.” Those subregions with low search volumes for “HPV vaccine” included Fukushima, Saga, Okinawa, Wakayama, and Aichi prefectures. In addition, subregions including Ishikawa, Tottori, Kyoto, Shizuoka, and Nagano prefectures displayed low interest in “cervical screening.” Relevant authorities should enhance dissemination of HPV vaccine and cervical cancer awareness in these sub-regions. Encouragingly, in the latest briefing on HPV vaccination, the MHLW recommended cooperation among regions and the establishment of consultants to promote vaccination [39]. Although search interest in “cervical cancer” and “cervical screening” was strongly correlated with the actual number of cervical cancer cases, we did not find a similar situation for the subregion interests. We speculated that this might be attributed to a deviation in regional-level searches from locations where cervical cancer was diagnosed. Nevertheless, Google Trends search data still serves as a useful tool for understanding the public interest for a particular topic in different subregions.

Conclusions

We conducted a chronological and geographical analysis of public interest in “cervical cancer,” “HPV vaccine,” and “cervical screening” topics using Google Trends data. Public search interest coincided with critical policies announced by the government, maintaining low interest in “HPV vaccine” from 2013 to 2020, while interest in “cervical cancer” and “cervical screening” was relatively high. Encouragingly, the Japanese public reignited interest in the HPV vaccine in 2020, which is expected to lower rates of cervical cancer. Google Trends can extend unique perspectives for authorities to absorb public concerns promptly, but it is limited in its interpretations of subregions.

Limitations

While this study explored the public search interest regarding cervical cancer in Japan, several limitations should be considered. First, the findings only reflect interests from people who utilize Google search and have access to internet information, which may not fully reflect the general population’s interests [40,41]. Nevertheless, given that the HPV vaccine is recommended for women younger than 45 in Japan, analyzing web search data helps to understand the target group’s concerns. Second, demographic features of Internet users cannot be established because the Google Trends system automatically anonymizes users using these search volumes [42]. Third, the search terms “cervical cancer,” “HPV vaccine,” and “cervical screening” inputted into Google Trends did not represent all search terms from public use. Finally, search interest analysis is a substitute method for public information-seeking interests that cannot replace traditional research methods. Multiple methods should be employed and integrated to provide more dimensional research information for a comprehensive understanding of public interest in cervical cancer, or for multiple VPDs which may benefit from Google Trends research, such as influenza, hepatitis B virus infection, tuberculosis and mumps, and etc. 

Declarations

Ethics Approval: We present our analysis without identifying specific individuals. Therefore, this study was exempt from review by the institutional review board because the activities described did not meet the requirements of human subjects’ research.

Consent for Publication: Not applicable

Availability of Data and Materials: We used publicly available data published by Google Trends and the National Cancer Center, Japan. All data generated or analyzed during this study are included in this published article (and its supplementary information files). 

Competing Interests: The authors declare that they have no competing interest.

Funding: This work was supported by the Japan Science and Technology (JST) Support for Pioneering Research Initiated by the Next Generation (SPRING; grant number JPMJSP2110).

Authors’ Contributions:  All authors contributed to this study. QN, JYL, MNT and TA designed the study. QN, AK, YY and SN collected the data. QN and JYL participated in data analysis and interpretation. MNT and TA contributed to interpretation of data. QN and JYL were involved in writing the manuscript. All authors read and reviewed the manuscript. The authors read and approved the final manuscript.

 

Acknowledgements: Not applicable

Abbreviations

WHO

World Health Organization

HPV

human papillomavirus

MHLW

Ministry of Health, Labour and Welfare

VPDs

vaccine-preventable disease

DALY

disability-adjusted life year

NCCJ

National Cancer Center, Japan

RSV

relative search volume

PELT

pruned exact linear time

LDP

Liberal Democratic Party

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