Questionnaire Survey on Cervical Cancer Screening and HPV Awareness among Patients at a Local Cancer Center in Japan

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Human papillomavirus (HPV) vaccination and cancer screening are crucially involved in the prevention of cancer-related mortality. However, in 2022, the cervical cancer screening rate in Japan was only ≈43.6%. This study aimed to conduct an epidemiological analysis of cervical cancer by collecting data from individual patients. 【Methods】A questionnaire survey was administered to patients who visited our hospital between January 2017 and July 2023 due to abnormal cervical cytological findings or a cancer diagnosis. Patients answered questions regarding their history of cervical cancer screening as well as knowledge of HPV and cervical cancer. 【Results】During the study period, 471 patients participated in the survey, with 35 declining to participate. Patients with Stage 1b1–4b primarily sought medical attention due to self-reported symptoms (P<0.001); however, they were less likely to have undergone cervical cancer screening (P<0.001). Additionally, older patients were less likely to be aware of the association of HPV with cervical and other cancers. Notably, 28 out of 129 patients with stage 1b1–4b cancer underwent cervical cancer screening within 2 years. The tumor location within the endocervical canal emerged as a significant factor contributing to false-negative results; further, non- squamous cell carcinoma (SCC) histology was another possible factor. 【Conclusions】Our findings suggest the need to widely disseminate information regarding the significance of cancer screening in order to increase cancer screening rates. Moreover, it is important to establish strategies for minimizing false-negative results in screening for non-SCC and endo-cervical canal tumors. Cervical Cancer Screening HPV Active recruitment strategy Introduction In 2020, the World Health Organization issued a statement to eliminate cervical cancer through human papillomavirus (HPV) vaccination, highly accurate cancer screening, and effective treatment of pre-invasive and invasive cancers [ 1 ]. In Japan, the incidence of cervical cancer has been increasing since 2000 [ 2 ], with this trend being in contrast to that in other developed countries. HPV vaccination and cervical cancer screening crucially contribute towards prevention of cancer-related mortality. The Japanese government subsidy for HPV vaccination of girls aged 13–16 years began in 2010. However, since June 2013, HPV vaccination was suspended due to repeated media reports regarding its adverse effects [ 3 ], which led a decrease in vaccine coverage from 68.9% for individuals born in 1999 to 0.2% for individuals born in 2003 [ 4 , 5 ]. After a 9-year suspension, the Ministry of Health, Labor, and Welfare of Japan announced the resumption of HPV vaccination [ 6 ]; further, it was resumed in local municipalities in April 2022. Contrastingly, Australia, which is among the highly advanced countries with early and extensive HPV vaccination coverage, has achieved a clear reduction in the incidence of cervical neoplasia [ 7 ]. In Japan, the efficacy of HPV vaccination has been demonstrated [ 8 ]. Despite numerous efforts towards resumption of HPV vaccination, Japan requires a large amount of time to achieve a significant decrease in the incidence of cervical cancer incidence through extensive countrywide vaccine coverage. Additionally, cervical cancer screening for detection of pre-cancerous lesions has been shown to reduce the occurrence of invasive cancer in USA [ 9 ] and Japan [ 10 ]. In Japan, eligible women aged 20–69 years receive an invitation letter for cervical cancer screening from local governments every 2 years as per the Japan cervical cancer screening guidelines [ 11 ]. Therefore, most women have a chance to undergo screening; moreover, some women undergo either workplace-provided or opportunistic screening. Despite the adoption of a robust screening program in the 1980s, the screening rate in Japan has been substantially lower than that in Western countries. Accordingly OECD Health Statistics 2023, 42.4% of women aged 20–69 years in Japan underwent a Pap smear test, which is lower than the > 70% rate among targeted women in Sweden, the USA, and the UK [ 12 ]. Various factors may impede screening, including cost, busy daily lifestyle, health illiteracy, and inadequate information regarding cervical cancer. Taken together, it important to increase the screening rate in Japan. Therefore, this study aimed to conduct a questionnaire survey of patients who visited our hospital with suspected cervical neoplasia or a cancer diagnosis. The study objectives were as follows: i) to understand the demographic characteristics of patients, ii) to assess patients’ knowledge regarding cervical cancer and HPV, iii) to identify weaknesses in the current strategy for cancer screening, and iv) to inform strategic improvements for increasing the screening rate. Methods A questionnaire survey was administered to patients who visited our hospital between January 2017 and December 2023 due to abnormal cervical cytological findings or a cancer diagnosis. In Japan, there are three options for cervical cancer screening: organized screening for eligible individuals aged > 20 years at 2-year intervals, periodic health checkups provided in the workplace as a benefit package, and opportunistic screening sought individually. After the Bethesda system was applied for cervical cancer screening in our medical district, a cone-shaped brush was primarily used to obtain samples for liquid-based cytology. Patients provided written informed consent and provided responses regarding their history of cervical cancer screening as well as knowledge of HPV and cervical cancer. This study was approved by the Ethics Committee of Gunma Prefectural Cancer Center (approval # 405–04064). Moreover, this study was conducted in accordance with relevant guidelines and regulations (Declaration of Helsinki). Responses were analyzed with respect to cervical cancer status using descriptive analysis methods, including the Kruskal-Wallis test, chi-square test, logistic analysis, and Fisher’s exact test. All statistical analyses were performed using EZR version 1.55 [ 13 ]. Results From January 2017 to December 2023, 471 patients were included in this study, while 35 individuals declined to participate. All patients were transferred to our hospital due to abnormal cytological findings, suspected cancer, or a diagnosis of cervical cancer. At the initial visit, 68 patients exhibited no lesions. However, 79, 195, 38, and 91 patients had CIN1–2, CIN3- the International Federation of Gynecology and Obstetrics (FIGO 2018) Stage1a, Stage 1b1 cervical cancer, and Stage 1b2-4b cervical cancer, respectively (Table 1). Among patients aged 20–29 years, none of the patients were diagnosed with Stage 1b1 and Stage 1b2-4b. However, there was a distinct proportion of patients with advanced cervical cancer (Stage 1b2-4b) in the elder age group, especially those aged ≥ 50 years. Patients with Stage 1b1-4b primarily visited our hospital because of self-reported symptoms, including vaginal bleeding and abnormal discharge. Contrastingly, patients with no lesions, CIN1-2, and CIN3-Stage 1a were mainly referred with abnormal cytological results (P < 0.001). In contrast to no lesions and CIN1–2, patients with Stage 1b1 and Stage 1b2–4b cervical cancer had a longer interval of cancer screening or had never undergone it (P < 0.001). In all age groups, most patients underwent cancer screening following invitation letters from local municipalities, followed by in health-checkup programs provided in the workplace (Table 2). Subsequently, we examined the association between cervical lesions and age at first screening (Table 3). We found that a significant proportion of patients in Stage 1b2-4b started cancer screening at an age ≥ 50 years. In all age groups, there was low awareness regarding the peak incidence age of cervical cancer and the fact that smoking was a risk factor for cervical cancer (Table 4). Many patients were aware of the absence of clinical symptoms of early-stage cervical cancer and the effectiveness of cervical cancer screening during their visit to our hospital but not at the screening visit (Table 2). Furthermore, older patients were less likely to recognize HPV as sexually transmitted and its association with cervical cancer. Moreover, most patients were unaware of the association of HPV with other cancers, including vulvar, anal, and mesopharyngeal cancers. Notably, 28 out of 129 patients with Stage 1b1-4b underwent cervical cancer screening within 2 years; further, 60.7% of these patients had a tumor size > 2 cm. Tumor location within the endocervical canal and non-SCC histology emerged as factors significantly contributing to false-negative screening results. Discussion Our findings indicated that patients who had never undergone cervical cancer screening or had long intervals between screening were at a higher risk of advanced cervical cancer than those who underwent regular screenings. Furthermore, patients who underwent screening had low awareness regarding the significance of screening; however, most of them were aware of this after being referred to our hospital. Notably, tumor location within the endo-cervical canal and non-SCC histology impeded detection of pre-cancerous or early-stage cancer through cervical cancer screening, even with 2-year intervals. These findings suggest the need to reconsider the strategies for screening participation and accuracy. As shown in Table 1, patients with invasive cancer who had long intervals between cancer screening or had never undergone cancer screening tended to present advanced disease at the time of diagnosis. This is consistent with previous reports demonstrating that > 50% of patients with cervical cancer never underwent screening or had longer-than-recommended intervals between screenings [ 14 , 15 ]. Despite extensive efforts in screening programs, the screening rates have remained relatively low. A systematic review showed that organized screening was more effective than opportunistic screening [ 16 ]. In our region, local municipalities send an invitation letter to eligible people every 2 years, with those who miss the screening receiving the same letter the following year; however, the screening rate remained low at 42.5% in 2022. Therefore, although organized screening may increase the screening rate to some extent, it was not to a satisfactory level in our medical district. Some studies have highlighted the economic-social barriers to cancer screening, and organized screening could reduce inequity [ 17 , 18 ]. However, one study reported that household income was not associated with screening rates [ 19 ]. This could be attributed to the fact that patients are required to pay 5–10 US dollars out of pocket owing to subsidies provided by the local government. Furthermore, a USA population-based assessment of cervical cancer screening showed that Asian people were less likely to undergo appropriately timed screening compared with White women [ 15 ], which suggests that ethnic culture might affect motivation for screening. Taken together, these findings suggest that increasing the screening rate requires a novel recruitment strategy. In this study, invitation letters were the reason for organized screening among ≈ 50% of the patients who had undergone screening; moreover, ≈ 20% of patients experienced screening provided at the workplace. However, patients in all age groups were hardly aware of the significance of screening (Table 2). As shown in Table 4, after visiting our hospital, most patients became aware of the lack of clinical symptoms at an early stage and the effectiveness of cancer screening, regardless of their age and screening history. Furthermore, individuals (especially those who were elder) had insufficient knowledge regarding HPV, including its transmission route; rate of transmission; effectiveness of vaccination; and association with cervical cancer and other cancers, including vulva, anal, and mesopharyngeal cancers. In the British colorectal cancer screening program, an information booklet about colorectal cancer is sent to eligible people along with the invitation letter. However, 22% of eligible individuals never read this booklet; moreover, 63% and 4% of individuals without and with a screening history never read this booklet, respectively [ 20 ]. This indicates that simply sending information regarding cervical cancer and the significance of screening may not effectively incentivize eligible individuals to undergo screening. A previous review found that tailored messages could alter women’s decisions regarding screening participation [ 21 ]; furthermore, primary care physicians who can provide familial messages to patients may remove barriers impeding screening participation [ 22 ]. Consequently, if possible, in-person conveyance of messages to patients is crucial for promoting health literacy by utilizing available resources, including the primary doctor, phone calls from the screening organizer, and educational events within the local community. The age of eligibility for cervical cancer screening is another important factor. Both the American College of Obstetricians and Gynecologists recommendation [ 23 ] the Ministry of Health, Labor and Welfare in Japan recommend initiation of cervical cancer screening at an age ≥ 20 years every 2 years. This is because invasive cancer is rare among patients aged < 20 years, with the age-adjusted incidence rate of cervical neoplasm peaking at the age of ≈ 40 years. In our study (Table 3), patients who started screening at a younger age were more likely to be diagnosed with at least CIN or early invasive cancer than patients who began screening at an older age. In Australia, where the HPV vaccination program was launched in 2007, a recent simulation based on the declining incidence of cervical neoplasm suggested that the age-adjusted annual incidence of cervical cancer would be as low as four cases in 10,000 women by 2028 with maintenance of the HPV vaccination and HPV testing program [ 24 ]. In our study, none of the patients aged 20–29 years was diagnosed with Stage Ib1-4b’ accordingly, expanding the HPV vaccination coverage could reduce the screening frequency among younger generations within a few decades, even in Japan. However, there is controversy regarding the age at which screening is no longer beneficial in older adults. The US Preventive Services Task Force does not recommend routine screening for women aged ≥ 65 years who have normal Pap smear test results and adequately adhered to screening [ 25 ]. In a Canadian modeling study utilizing registry and survey data, the lifetime risk of cervical cancer in individuals whose screening history was unknown at the age of 70 years could be reduced from 1/158 to 1/1206 by recall for screening [ 26 ]. Moreover, Swedish cancer registry data demonstrated that regular screening reduced the cancer risk among individuals aged ≥ 65 years [ 27 ]. Taken together with our findings that elder individuals account for a considerable high percentage of patients with invasive cervical cancers, older people should be encouraged to undergo screening until the HPV-vaccinated generation reaches old age. In our study, 28 out of 129 patients with Stage 1b1-4b underwent cervical cancer screening within 2 years; further, 60.7% of these patients had a tumor size > 2 cm (Table 5). There was a nearly significant difference in histology findings between patients who had their last screening within 2 years and those with longer intervals. In this study, 9 out of 13 patients who had their last screening within 2 years were aged < 50 years and had non-SCC histology at diagnosis. In patients within this age group, squamocolumnar junction (SC-junction), from which cervical cancer arises, is usually located outside the cervix, and thus allows relatively easy sampling. Previous studies have suggested that cytology has low sensitivity for detecting precancerous lesions of adenocarcinoma [ 28 , 29 ]; moreover, there is an increase in the worldwide incidence rate of adenocarcinoma against SCC, especially among younger patients [ 30 ]. Given that the HPV-positive rate among patients with adenocarcinoma is ≈ 90% [ 31 ], the younger generation could be a good candidate for HPV-based screening. However, HPV infection can be transient and CIN can be regressive in younger people. Therefore, patients with HPV-positive results who have negative cytology should adhere to the next HPV test at an adequate interval to avoid unnecessary colposcopy and biopsy, which is further supported by previous findings that a 5-year interval of the HPV test is safer than a 3-year interval of cytology [ 32 ]. Tumor location was another significant factor in patients diagnosed within two 2 years of screening. In this study, six out of eight patients with tumors located in the end-cervical canal and a screening interval of ≤2 years were aged > 50 years. Assuming that the SC-junction migrates toward the deep endocervical canal after menopause, the efficacy of cytological screening in these individuals may be lower than that in younger people [ 33 ]. As year of 2021, 48 countries have adopted HPV-based screening for primary method [ 34 ]. However, the Catalan Institute investigated the HPV genotype in 10,575 cases which demonstrated that HPV was detected 87% in squamous carcinoma and 62% in adenocarcinoma [ 35 ] and lower HPV positive in older patients [ 36 ]. Consistent with previous findings [ 37 ], we found that transvaginal ultrasound examination with a Doppler scan can easily detect cervical lesions. Although the cost-benefit balance must be considered, ultrasound examination with cytology screening could be a tailored option for some patients undergoing cancer screening. Finally, physicians must remind their patients that screening results may be inaccurate. Therefore, even with a negative screening result, patients with self-reported symptoms should consult a physician. Otherwise, a false negative result may lead to advanced disease. Conclusions It is important to increase the rate and efficacy of cervical cancer screening in order to prevent cervical cancer mortality. In Japan, both cancer screening and HPV vaccination rates are low. Accordingly, cancer screening is expected to play a crucial role in the detection of cancer precursors in the coming decades. Another important step is improving the precision of screening in order to avoid false-negative findings. Although cytological screening has significantly reduced the incidence and mortality of cervical cancer, HPV-based screening may replace it in the future. Continuous monitoring of the incidence and mortality among different patient groups may inform the development of efficient screening strategies. Abbreviations HPV, Human papillomavirus; SCC, squamous cell carcinoma ; CIN, cervical intraepithelial neoplasia; FIGO, International Federation of Gynecology and Obstetrics; SC-junction, squamocolumnar junction Declarations Ethics approval and consent to participate: This study was approved by the Ethics Committee of Gunma Prefectural Cancer Center (approval # 405-04064). All methods were performed in accordance with relevant guidelines and regulations (Declaration of Helsinki). Informed consent was obtained from all study participants. Consent for publication: Not applicable. Availability of data and materials: The data used in this study are available from corresponding author on reasonable request. Competing interests: The authors declare that they have no competing interests. Funding: This study was not supported by any funding source. Acknowledgement: We appreciate Dr. Kitahara (Gunma University) for his technical advice on statistical analyses. Author contributions: K.N. planned and designed the study, drafted the manuscript, and statistically analyzed the data. K.N., K.K., T.N,and S.Y. collected the patients’ data. References WHO. Global strategy to accelerate the elimination of cervical cancer as a public health problem. Nov 17, 2020. https://www.who . int/publications-detail-redirect/9789240014107 . 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Pirog EC, Lloveras B, Molijn A, Tous S, Guimera N, Alejo M, Clavero O, Klaustermeier J, Jenkins D, Quint WG et al : HPV prevalence and genotypes in different histological subtypes of cervical adenocarcinoma, a worldwide analysis of 760 cases . Mod Pathol 2014, 27 (12):1559-1567. Oh H, Park SB, Park HJ, Lee ES, Hur J, Choi W, Choi BI: Ultrasonographic features of uterine cervical lesions . Br J Radiol 2021, 94 (1121):20201242. Tables Tables are available in the Supplementary Files section. Additional Declarations No competing interests reported. Supplementary Files TableNakamuraetal.xlsx Cite Share Download PDF Status: Published Journal Publication published 16 Jul, 2024 Read the published version in BMC Women's Health → Version 1 posted Editorial decision: Revision requested 20 Jun, 2024 Editor assigned by journal 19 Jun, 2024 Submission checks completed at journal 19 Jun, 2024 First submitted to journal 19 Jun, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4608168","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":316670119,"identity":"4e68cc03-87a3-414c-87f1-920b510f560c","order_by":0,"name":"Kazuto Nakamura","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAAz0lEQVRIiWNgGAWjYDACHgglhyR0gBgtCQzGpGtJbCDaXeY8hx9/5v1hkz4/Ivfohh8MdvIMjGfxW2PZ22ZgzJOQlrvxRl7azR6GZMMGhnMJeLUYnGcwSOZJOJy7cUaO2Q3efweAys8YENDC/uEwUEu6IVDLzT8MxGg522PYDNSSIC+RY3abhygtZ84UM85JSzPcwPPG7LYM0C9tBP1yJn3zhzc2NvLy7UCHvQGGGL8EgRBD6IWpY5M4Q5wOBvkGGIu/h0gto2AUjIJRMFIAANfqRuFaisImAAAAAElFTkSuQmCC","orcid":"","institution":"Gunma Prefectural Cancer Center","correspondingAuthor":true,"prefix":"","firstName":"Kazuto","middleName":"","lastName":"Nakamura","suffix":""},{"id":316670121,"identity":"361de390-fbd9-485c-879c-a0c5c78588ed","order_by":1,"name":"Keiko Kigure","email":"","orcid":"","institution":"Gunma Prefectural Cancer Center","correspondingAuthor":false,"prefix":"","firstName":"Keiko","middleName":"","lastName":"Kigure","suffix":""},{"id":316670122,"identity":"e86f7f9a-ab67-4386-b81c-aa5137d92958","order_by":2,"name":"Toshio Nishimura","email":"","orcid":"","institution":"Gunma Prefectural Cancer Center","correspondingAuthor":false,"prefix":"","firstName":"Toshio","middleName":"","lastName":"Nishimura","suffix":""},{"id":316670123,"identity":"adb57208-f199-4445-8d58-cf895bbd7b74","order_by":3,"name":"Soichi Yamashita","email":"","orcid":"","institution":"Gunma Prefectural Cancer Center","correspondingAuthor":false,"prefix":"","firstName":"Soichi","middleName":"","lastName":"Yamashita","suffix":""}],"badges":[],"createdAt":"2024-06-19 22:56:14","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4608168/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4608168/v1","draftVersion":[],"editorialEvents":[{"content":"https://doi.org/10.1186/s12905-024-03256-z","type":"published","date":"2024-07-16T16:13:09+00:00"}],"editorialNote":"","failedWorkflow":false,"files":[{"id":61595268,"identity":"eaf52f54-edc6-4899-88d4-cf9eec7c925d","added_by":"auto","created_at":"2024-08-01 17:21:42","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1332651,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4608168/v1/e5a5f379-87ff-4790-9f92-57d4d8ad23bd.pdf"},{"id":59949840,"identity":"64a92b26-c5d0-49a8-892d-8c0159264aaa","added_by":"auto","created_at":"2024-07-09 17:14:32","extension":"xlsx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":28440,"visible":true,"origin":"","legend":"","description":"","filename":"TableNakamuraetal.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-4608168/v1/fbfd30fad9579f22dcef3a8f.xlsx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Questionnaire Survey on Cervical Cancer Screening and HPV Awareness among Patients at a Local Cancer Center in Japan","fulltext":[{"header":"Introduction","content":"\u003cp\u003eIn 2020, the World Health Organization issued a statement to eliminate cervical cancer through human papillomavirus (HPV) vaccination, highly accurate cancer screening, and effective treatment of pre-invasive and invasive cancers [\u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e1\u003c/span\u003e]. In Japan, the incidence of cervical cancer has been increasing since 2000 [\u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2\u003c/span\u003e], with this trend being in contrast to that in other developed countries. HPV vaccination and cervical cancer screening crucially contribute towards prevention of cancer-related mortality. The Japanese government subsidy for HPV vaccination of girls aged 13\u0026ndash;16 years began in 2010. However, since June 2013, HPV vaccination was suspended due to repeated media reports regarding its adverse effects [\u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e], which led a decrease in vaccine coverage from 68.9% for individuals born in 1999 to 0.2% for individuals born in 2003 [\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e]. After a 9-year suspension, the Ministry of Health, Labor, and Welfare of Japan announced the resumption of HPV vaccination [\u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e6\u003c/span\u003e]; further, it was resumed in local municipalities in April 2022. Contrastingly, Australia, which is among the highly advanced countries with early and extensive HPV vaccination coverage, has achieved a clear reduction in the incidence of cervical neoplasia [\u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e7\u003c/span\u003e]. In Japan, the efficacy of HPV vaccination has been demonstrated [\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e]. Despite numerous efforts towards resumption of HPV vaccination, Japan requires a large amount of time to achieve a significant decrease in the incidence of cervical cancer incidence through extensive countrywide vaccine coverage.\u003c/p\u003e \u003cp\u003eAdditionally, cervical cancer screening for detection of pre-cancerous lesions has been shown to reduce the occurrence of invasive cancer in USA [\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e] and Japan [\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e]. In Japan, eligible women aged 20\u0026ndash;69 years receive an invitation letter for cervical cancer screening from local governments every 2 years as per the Japan cervical cancer screening guidelines [\u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e11\u003c/span\u003e]. Therefore, most women have a chance to undergo screening; moreover, some women undergo either workplace-provided or opportunistic screening. Despite the adoption of a robust screening program in the 1980s, the screening rate in Japan has been substantially lower than that in Western countries. Accordingly OECD Health Statistics 2023, 42.4% of women aged 20\u0026ndash;69 years in Japan underwent a Pap smear test, which is lower than the \u0026gt;\u0026thinsp;70% rate among targeted women in Sweden, the USA, and the UK [\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e]. Various factors may impede screening, including cost, busy daily lifestyle, health illiteracy, and inadequate information regarding cervical cancer.\u003c/p\u003e \u003cp\u003eTaken together, it important to increase the screening rate in Japan. Therefore, this study aimed to conduct a questionnaire survey of patients who visited our hospital with suspected cervical neoplasia or a cancer diagnosis. The study objectives were as follows: i) to understand the demographic characteristics of patients, ii) to assess patients\u0026rsquo; knowledge regarding cervical cancer and HPV, iii) to identify weaknesses in the current strategy for cancer screening, and iv) to inform strategic improvements for increasing the screening rate.\u003c/p\u003e"},{"header":"Methods","content":"\u003cp\u003eA questionnaire survey was administered to patients who visited our hospital between January 2017 and December 2023 due to abnormal cervical cytological findings or a cancer diagnosis. In Japan, there are three options for cervical cancer screening: organized screening for eligible individuals aged\u0026thinsp;\u0026gt;\u0026thinsp;20 years at 2-year intervals, periodic health checkups provided in the workplace as a benefit package, and opportunistic screening sought individually. After the Bethesda system was applied for cervical cancer screening in our medical district, a cone-shaped brush was primarily used to obtain samples for liquid-based cytology.\u003c/p\u003e \u003cp\u003ePatients provided written informed consent and provided responses regarding their history of cervical cancer screening as well as knowledge of HPV and cervical cancer. This study was approved by the Ethics Committee of Gunma Prefectural Cancer Center (approval # 405\u0026ndash;04064). Moreover, this study was conducted in accordance with relevant guidelines and regulations (Declaration of Helsinki). Responses were analyzed with respect to cervical cancer status using descriptive analysis methods, including the Kruskal-Wallis test, chi-square test, logistic analysis, and Fisher\u0026rsquo;s exact test. All statistical analyses were performed using EZR version 1.55 [\u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e13\u003c/span\u003e].\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eFrom January 2017 to December 2023, 471 patients were included in this study, while 35 individuals declined to participate. All patients were transferred to our hospital due to abnormal cytological findings, suspected cancer, or a diagnosis of cervical cancer. At the initial visit, 68 patients exhibited no lesions. However, 79, 195, 38, and 91 patients had CIN1\u0026ndash;2, CIN3- the International Federation of Gynecology and Obstetrics (FIGO 2018) Stage1a, Stage 1b1 cervical cancer, and Stage 1b2-4b cervical cancer, respectively (Table\u0026nbsp;1). Among patients aged 20\u0026ndash;29 years, none of the patients were diagnosed with Stage 1b1 and Stage 1b2-4b. However, there was a distinct proportion of patients with advanced cervical cancer (Stage 1b2-4b) in the elder age group, especially those aged\u0026thinsp;\u0026ge;\u0026thinsp;50 years. Patients with Stage 1b1-4b primarily visited our hospital because of self-reported symptoms, including vaginal bleeding and abnormal discharge. Contrastingly, patients with no lesions, CIN1-2, and CIN3-Stage 1a were mainly referred with abnormal cytological results (P\u0026thinsp;\u0026lt;\u0026thinsp;0.001). In contrast to no lesions and CIN1\u0026ndash;2, patients with Stage 1b1 and Stage 1b2\u0026ndash;4b cervical cancer had a longer interval of cancer screening or had never undergone it (P\u0026thinsp;\u0026lt;\u0026thinsp;0.001). In all age groups, most patients underwent cancer screening following invitation letters from local municipalities, followed by in health-checkup programs provided in the workplace (Table\u0026nbsp;2). Subsequently, we examined the association between cervical lesions and age at first screening (Table\u0026nbsp;3). We found that a significant proportion of patients in Stage 1b2-4b started cancer screening at an age\u0026thinsp;\u0026ge;\u0026thinsp;50 years. In all age groups, there was low awareness regarding the peak incidence age of cervical cancer and the fact that smoking was a risk factor for cervical cancer (Table\u0026nbsp;4). Many patients were aware of the absence of clinical symptoms of early-stage cervical cancer and the effectiveness of cervical cancer screening during their visit to our hospital but not at the screening visit (Table\u0026nbsp;2). Furthermore, older patients were less likely to recognize HPV as sexually transmitted and its association with cervical cancer. Moreover, most patients were unaware of the association of HPV with other cancers, including vulvar, anal, and mesopharyngeal cancers. Notably, 28 out of 129 patients with Stage 1b1-4b underwent cervical cancer screening within 2 years; further, 60.7% of these patients had a tumor size\u0026thinsp;\u0026gt;\u0026thinsp;2 cm. Tumor location within the endocervical canal and non-SCC histology emerged as factors significantly contributing to false-negative screening results.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eOur findings indicated that patients who had never undergone cervical cancer screening or had long intervals between screening were at a higher risk of advanced cervical cancer than those who underwent regular screenings. Furthermore, patients who underwent screening had low awareness regarding the significance of screening; however, most of them were aware of this after being referred to our hospital. Notably, tumor location within the endo-cervical canal and non-SCC histology impeded detection of pre-cancerous or early-stage cancer through cervical cancer screening, even with 2-year intervals. These findings suggest the need to reconsider the strategies for screening participation and accuracy.\u003c/p\u003e \u003cp\u003eAs shown in Table\u0026nbsp;1, patients with invasive cancer who had long intervals between cancer screening or had never undergone cancer screening tended to present advanced disease at the time of diagnosis. This is consistent with previous reports demonstrating that \u0026gt;\u0026thinsp;50% of patients with cervical cancer never underwent screening or had longer-than-recommended intervals between screenings [\u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e14\u003c/span\u003e, \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e]. Despite extensive efforts in screening programs, the screening rates have remained relatively low. A systematic review showed that organized screening was more effective than opportunistic screening [\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e]. In our region, local municipalities send an invitation letter to eligible people every 2 years, with those who miss the screening receiving the same letter the following year; however, the screening rate remained low at 42.5% in 2022. Therefore, although organized screening may increase the screening rate to some extent, it was not to a satisfactory level in our medical district. Some studies have highlighted the economic-social barriers to cancer screening, and organized screening could reduce inequity [\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e, \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e18\u003c/span\u003e]. However, one study reported that household income was not associated with screening rates [\u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e19\u003c/span\u003e]. This could be attributed to the fact that patients are required to pay 5\u0026ndash;10 US dollars out of pocket owing to subsidies provided by the local government. Furthermore, a USA population-based assessment of cervical cancer screening showed that Asian people were less likely to undergo appropriately timed screening compared with White women [\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e], which suggests that ethnic culture might affect motivation for screening. Taken together, these findings suggest that increasing the screening rate requires a novel recruitment strategy.\u003c/p\u003e \u003cp\u003eIn this study, invitation letters were the reason for organized screening among \u0026asymp;\u0026thinsp;50% of the patients who had undergone screening; moreover, \u0026asymp;\u0026thinsp;20% of patients experienced screening provided at the workplace. However, patients in all age groups were hardly aware of the significance of screening (Table\u0026nbsp;2). As shown in Table\u0026nbsp;4, after visiting our hospital, most patients became aware of the lack of clinical symptoms at an early stage and the effectiveness of cancer screening, regardless of their age and screening history. Furthermore, individuals (especially those who were elder) had insufficient knowledge regarding HPV, including its transmission route; rate of transmission; effectiveness of vaccination; and association with cervical cancer and other cancers, including vulva, anal, and mesopharyngeal cancers. In the British colorectal cancer screening program, an information booklet about colorectal cancer is sent to eligible people along with the invitation letter. However, 22% of eligible individuals never read this booklet; moreover, 63% and 4% of individuals without and with a screening history never read this booklet, respectively [\u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e20\u003c/span\u003e]. This indicates that simply sending information regarding cervical cancer and the significance of screening may not effectively incentivize eligible individuals to undergo screening. A previous review found that tailored messages could alter women\u0026rsquo;s decisions regarding screening participation [\u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e21\u003c/span\u003e]; furthermore, primary care physicians who can provide familial messages to patients may remove barriers impeding screening participation [\u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e22\u003c/span\u003e]. Consequently, if possible, in-person conveyance of messages to patients is crucial for promoting health literacy by utilizing available resources, including the primary doctor, phone calls from the screening organizer, and educational events within the local community.\u003c/p\u003e \u003cp\u003eThe age of eligibility for cervical cancer screening is another important factor. Both the American College of Obstetricians and Gynecologists recommendation [\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e23\u003c/span\u003e] the Ministry of Health, Labor and Welfare in Japan recommend initiation of cervical cancer screening at an age\u0026thinsp;\u0026ge;\u0026thinsp;20 years every 2 years. This is because invasive cancer is rare among patients aged\u0026thinsp;\u0026lt;\u0026thinsp;20 years, with the age-adjusted incidence rate of cervical neoplasm peaking at the age of \u0026asymp;\u0026thinsp;40 years. In our study (Table\u0026nbsp;3), patients who started screening at a younger age were more likely to be diagnosed with at least CIN or early invasive cancer than patients who began screening at an older age. In Australia, where the HPV vaccination program was launched in 2007, a recent simulation based on the declining incidence of cervical neoplasm suggested that the age-adjusted annual incidence of cervical cancer would be as low as four cases in 10,000 women by 2028 with maintenance of the HPV vaccination and HPV testing program [\u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e24\u003c/span\u003e]. In our study, none of the patients aged 20\u0026ndash;29 years was diagnosed with Stage Ib1-4b\u0026rsquo; accordingly, expanding the HPV vaccination coverage could reduce the screening frequency among younger generations within a few decades, even in Japan. However, there is controversy regarding the age at which screening is no longer beneficial in older adults. The US Preventive Services Task Force does not recommend routine screening for women aged\u0026thinsp;\u0026ge;\u0026thinsp;65 years who have normal Pap smear test results and adequately adhered to screening [\u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e25\u003c/span\u003e]. In a Canadian modeling study utilizing registry and survey data, the lifetime risk of cervical cancer in individuals whose screening history was unknown at the age of 70 years could be reduced from 1/158 to 1/1206 by recall for screening [\u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e26\u003c/span\u003e]. Moreover, Swedish cancer registry data demonstrated that regular screening reduced the cancer risk among individuals aged\u0026thinsp;\u0026ge;\u0026thinsp;65 years [\u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e27\u003c/span\u003e]. Taken together with our findings that elder individuals account for a considerable high percentage of patients with invasive cervical cancers, older people should be encouraged to undergo screening until the HPV-vaccinated generation reaches old age.\u003c/p\u003e \u003cp\u003eIn our study, 28 out of 129 patients with Stage 1b1-4b underwent cervical cancer screening within 2 years; further, 60.7% of these patients had a tumor size\u0026thinsp;\u0026gt;\u0026thinsp;2 cm (Table\u0026nbsp;5). There was a nearly significant difference in histology findings between patients who had their last screening within 2 years and those with longer intervals. In this study, 9 out of 13 patients who had their last screening within 2 years were aged\u0026thinsp;\u0026lt;\u0026thinsp;50 years and had non-SCC histology at diagnosis. In patients within this age group, squamocolumnar junction (SC-junction), from which cervical cancer arises, is usually located outside the cervix, and thus allows relatively easy sampling. Previous studies have suggested that cytology has low sensitivity for detecting precancerous lesions of adenocarcinoma [\u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e28\u003c/span\u003e, \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e29\u003c/span\u003e]; moreover, there is an increase in the worldwide incidence rate of adenocarcinoma against SCC, especially among younger patients [\u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e30\u003c/span\u003e]. Given that the HPV-positive rate among patients with adenocarcinoma is \u0026asymp;\u0026thinsp;90% [\u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e31\u003c/span\u003e], the younger generation could be a good candidate for HPV-based screening. However, HPV infection can be transient and CIN can be regressive in younger people. Therefore, patients with HPV-positive results who have negative cytology should adhere to the next HPV test at an adequate interval to avoid unnecessary colposcopy and biopsy, which is further supported by previous findings that a 5-year interval of the HPV test is safer than a 3-year interval of cytology [\u003cspan citationid=\"CR66\" class=\"CitationRef\"\u003e32\u003c/span\u003e]. Tumor location was another significant factor in patients diagnosed within two 2 years of screening. In this study, six out of eight patients with tumors located in the end-cervical canal and a screening interval of \u0026le;2 years were aged\u0026thinsp;\u0026gt;\u0026thinsp;50 years. Assuming that the SC-junction migrates toward the deep endocervical canal after menopause, the efficacy of cytological screening in these individuals may be lower than that in younger people [\u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e33\u003c/span\u003e]. As year of 2021, 48 countries have adopted HPV-based screening for primary method [\u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e34\u003c/span\u003e]. However, the Catalan Institute investigated the HPV genotype in 10,575 cases which demonstrated that HPV was detected 87% in squamous carcinoma and 62% in adenocarcinoma [\u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e35\u003c/span\u003e] and lower HPV positive in older patients [\u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e36\u003c/span\u003e]. Consistent with previous findings [\u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e37\u003c/span\u003e], we found that transvaginal ultrasound examination with a Doppler scan can easily detect cervical lesions. Although the cost-benefit balance must be considered, ultrasound examination with cytology screening could be a tailored option for some patients undergoing cancer screening. Finally, physicians must remind their patients that screening results may be inaccurate. Therefore, even with a negative screening result, patients with self-reported symptoms should consult a physician. Otherwise, a false negative result may lead to advanced disease.\u003c/p\u003e"},{"header":"Conclusions","content":"\u003cp\u003eIt is important to increase the rate and efficacy of cervical cancer screening in order to prevent cervical cancer mortality. In Japan, both cancer screening and HPV vaccination rates are low. Accordingly, cancer screening is expected to play a crucial role in the detection of cancer precursors in the coming decades. Another important step is improving the precision of screening in order to avoid false-negative findings. Although cytological screening has significantly reduced the incidence and mortality of cervical cancer, HPV-based screening may replace it in the future. Continuous monitoring of the incidence and mortality among different patient groups may inform the development of efficient screening strategies.\u003c/p\u003e"},{"header":"Abbreviations","content":"\u003cp\u003eHPV, Human papillomavirus; SCC, squamous cell carcinoma ; CIN, cervical intraepithelial neoplasia; FIGO, International Federation of Gynecology and Obstetrics; SC-junction, squamocolumnar junction\u0026nbsp;\u003c/p\u003e\n"},{"header":"Declarations","content":"\u003cp\u003eEthics approval and consent to participate:\u0026nbsp;This study was approved by\u0026nbsp;the Ethics Committee of Gunma Prefectural Cancer Center (approval #\u0026nbsp;405-04064). All methods were performed in accordance with relevant guidelines and regulations (Declaration of Helsinki).\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eInformed consent was obtained from all study participants. \u0026nbsp;\u003c/p\u003e\n\u003cp\u003eConsent for publication: Not applicable.\u003c/p\u003e\n\u003cp\u003eAvailability of data and materials:\u0026nbsp;\u0026nbsp;The data used in this study\u0026nbsp;are available from corresponding author on reasonable request.\u003c/p\u003e\n\u003cp\u003eCompeting interests: The authors declare that they have no competing interests.\u003c/p\u003e\n\u003cp\u003eFunding: This study was not supported by any funding source.\u003c/p\u003e\n\u003cp\u003eAcknowledgement: We appreciate Dr.\u0026nbsp;Kitahara (Gunma University) for his\u0026nbsp;technical advice on statistical analyses.\u003c/p\u003e\n\u003cp\u003eAuthor contributions: K.N. planned and designed the study, drafted the manuscript, and statistically analyzed the data. K.N., K.K., T.N,and S.Y. collected the patients\u0026rsquo; data.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003e\u003cstrong\u003eWHO. Global strategy to accelerate the elimination of cervical cancer as a public health problem. 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Robles C, Peremiquel-Trillas P, de Sanjose S, Bruni L: \u003cstrong\u003eWorldwide use of HPV self-sampling for cervical cancer screening\u003c/strong\u003e. \u003cem\u003ePrev Med \u003c/em\u003e2022, \u003cstrong\u003e154\u003c/strong\u003e:106900.\u003c/li\u003e\n\u003cli\u003ede Sanjose S, Quint WG, Alemany L, Geraets DT, Klaustermeier JE, Lloveras B, Tous S, Felix A, Bravo LE, Shin HR\u003cem\u003e et al\u003c/em\u003e: \u003cstrong\u003eHuman papillomavirus genotype attribution in invasive cervical cancer: a retrospective cross-sectional worldwide study\u003c/strong\u003e. \u003cem\u003eLancet Oncol \u003c/em\u003e2010, \u003cstrong\u003e11\u003c/strong\u003e(11):1048-1056.\u003c/li\u003e\n\u003cli\u003ePirog EC, Lloveras B, Molijn A, Tous S, Guimera N, Alejo M, Clavero O, Klaustermeier J, Jenkins D, Quint WG\u003cem\u003e et al\u003c/em\u003e: \u003cstrong\u003eHPV prevalence and genotypes in different histological subtypes of cervical adenocarcinoma, a worldwide analysis of 760 cases\u003c/strong\u003e. \u003cem\u003eMod Pathol \u003c/em\u003e2014, \u003cstrong\u003e27\u003c/strong\u003e(12):1559-1567.\u003c/li\u003e\n\u003cli\u003eOh H, Park SB, Park HJ, Lee ES, Hur J, Choi W, Choi BI: \u003cstrong\u003eUltrasonographic features of uterine cervical lesions\u003c/strong\u003e. \u003cem\u003eBr J Radiol \u003c/em\u003e2021, \u003cstrong\u003e94\u003c/strong\u003e(1121):20201242.\u003c/li\u003e\n\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables are available in the Supplementary Files section.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"bmc-womens-health","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmwh","sideBox":"Learn more about [BMC Women's Health](http://bmcwomenshealth.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmwh/default.aspx","title":"BMC Women's Health","twitterHandle":"","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true},"keywords":"Cervical Cancer, Screening, HPV, Active recruitment strategy","lastPublishedDoi":"10.21203/rs.3.rs-4608168/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4608168/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003e【Background】 The incidence of cervical intraepithelial neoplasia is increasing in Japan. Human papillomavirus (HPV) vaccination and cancer screening are crucially involved in the prevention of cancer-related mortality. However, in 2022, the cervical cancer screening rate in Japan was only ≈43.6%. This study aimed to conduct an epidemiological analysis of cervical cancer by collecting data from individual patients.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e【Methods】A questionnaire survey was administered to patients who visited our hospital between January 2017 and July 2023 due to abnormal cervical cytological findings or a cancer diagnosis. Patients answered questions regarding their history of cervical cancer screening as well as knowledge of HPV and cervical cancer.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e【Results】During the study period, 471 patients participated in the survey, with 35 declining to participate. Patients with Stage 1b1–4b primarily sought medical attention due to self-reported symptoms (P\u0026lt;0.001); however, they were less likely to have undergone cervical cancer screening (P\u0026lt;0.001). Additionally, older patients were less likely to be aware of the association of HPV with cervical and other cancers. Notably, 28 out of 129 patients with stage 1b1–4b cancer underwent cervical cancer screening within 2 years. The tumor location within the endocervical canal emerged as a significant factor contributing to false-negative results; further, non- squamous cell carcinoma (SCC) histology was another possible factor.\u003c/p\u003e\n\u003cp\u003e【Conclusions】Our findings suggest the need to widely disseminate information regarding the significance of cancer screening in order to increase cancer screening rates. Moreover, it is important to establish strategies for minimizing false-negative results in screening for non-SCC and endo-cervical canal tumors.\u003c/p\u003e","manuscriptTitle":"Questionnaire Survey on Cervical Cancer Screening and HPV Awareness among Patients at a Local Cancer Center in Japan","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-07-09 17:14:27","doi":"10.21203/rs.3.rs-4608168/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"Revision requested","date":"2024-06-20T05:00:44+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-06-20T00:23:27+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-06-20T00:22:54+00:00","index":"","fulltext":""},{"type":"submitted","content":"BMC Women's Health","date":"2024-06-19T22:54:59+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"bmc-womens-health","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":false,"externalIdentity":"bmwh","sideBox":"Learn more about [BMC Women's Health](http://bmcwomenshealth.biomedcentral.com/)","snPcode":"","submissionUrl":"https://www.editorialmanager.com/bmwh/default.aspx","title":"BMC Women's Health","twitterHandle":"","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"em","reportingPortfolio":"BMC Series","inReviewEnabled":true,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"2d46ddfc-42dd-473a-878d-6f8d6184f796","owner":[],"postedDate":"July 9th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[],"tags":[],"updatedAt":"2024-08-01T16:19:22+00:00","versionOfRecord":{"articleIdentity":"rs-4608168","link":"https://doi.org/10.1186/s12905-024-03256-z","journal":{"identity":"bmc-womens-health","isVorOnly":false,"title":"BMC Women's Health"},"publishedOn":"2024-07-16 16:13:09","publishedOnDateReadable":"July 16th, 2024"},"versionCreatedAt":"2024-07-09 17:14:27","video":"","vorDoi":"10.1186/s12905-024-03256-z","vorDoiUrl":"https://doi.org/10.1186/s12905-024-03256-z","workflowStages":[]},"version":"v1","identity":"rs-4608168","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4608168","identity":"rs-4608168","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}