Incidence, persistence, and clearance of cervical Human Papillomavirus among gynecological outpatients in Kunming, Yunnan, China from 2019-2023: A retrospective cohort study

Incidence, persistence, and clearance of cervical Human Papillomavirus among gynecological outpatients in Kunming, Yunnan, China from 2019-2023: A retrospective cohort study | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Incidence, persistence, and clearance of cervical Human Papillomavirus among gynecological outpatients in Kunming, Yunnan, China from 2019-2023: A retrospective cohort study Yafei Huang, Xiangcong Wei, Yan Guo, Ting Su, Qiuting Duan, Xin Fan, and 5 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4606669/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract Purpose Human papillomavirus (HPV) infection is the primary driver of cervical cancer development and progression. This study aimed to determine the incidence, persistence, and clearance of type-specific HPV infections in Yunnan. Methods A retrospective cohort study was conducted between October 2019 and August 2023 on female gynecological outpatients residing in Yunnan, Southwest China. HPV genotyping was performed using a multiplex polymerase chain reaction and capillary electrophoresis. We investigated the incidence, persistence, and clearance of HPV in women who tested again at various times following the initial test. Results This study included 45,149 participants; overall incidence of HPV infection was 36.84% with HPV 52 having the highest incidence, followed by HPV 51, 81, 58, and 16. The age ranges–30–39 and 40–49 y had the highest incidence rates. The overall persistence rate of the HPV infection was 55.56%, while HPV subtypes 42, 52, 58, 81, and 56 showed the highest rates of persistent infection. The highest rates of persistent infection were found in the 59 y age groups. The overall HPV clearance rate was 74.43%, and it increased with age. The most probable HPV subtypes to be cleared were 26, 83, 11, 82, and 44, least likely HR HPV subtypes were 58, 52, and 35, and least likely LR HPV subtypes were 42, 81, and 43. Conclusions Women in Yunnan had a higher likelihood of incident and persistent infections and a lower likelihood of being cleared of HPV 58, 52, 42, and 81. Older adults are more prone to persistent HPV infection, whereas younger individuals are more likely to recover from infection. Human Papillomavirus Incidence Persistence Clearance Yunnan Figures Figure 1 Figure 2 Figure 3 Figure 4 Figure 5 Introduction Human papillomavirus (HPV) causes one of the most prevalent sexually transmitted diseases (STDs) worldwide, which is the HPV infection. According to numerous studies till date, HPV infection plays a central role in the occurrence of cervical cancer[1]. Despite the promotion of prophylactic vaccination, vaccination rates remain low, especially in underdeveloped countries. Moreover, only a few antiviral therapies are available for HPV infections, with its burden on public health increasing. To date, more than 200 HPV genotypes have been identified; based on their association with cancer, HPV has been categorized into high-risk HPV(HR-HPV) and low-risk HPV(LR-HPV) genotypes. In the majority of HPV-infected individuals, the infection is cleared by the immune system within 1 or 2 years of onset. However, a small number of infected people have a persistent or latent infection status for years, which contributes to malignant transformation. Persistent HPV infection plays an important role in the occurrence of cervical, anogenital, and head and neck cancers [2, 3]. According to several studies, the detection of the same carcinogenic HPV type over time may be particularly crucial for cervical carcinogenesis [4, 5]. Regional and population-specific differences are observed in the incidence, persistence, and clearance rates of HPV [6–9]. In prepubertal girls and boys, HPV vaccination has proven to be highly successful in preventing HPV infection and associated illnesses with HPV infection [10]. Furthermore, China launched bivalent(2v), quadrivalent(4v), and nine-valent (9v) HPV vaccinations between July 2017 and the end of 2018[11]. Therefore, to better understand the local efficacy of HPV vaccination and provide a theoretical foundation for vaccination, a re-evaluation of the local rates of incidence, persistence, and clearance of HPV infections is required. The aim of the present study was to investigate the incidence, persistence, and clearance rates of HPV infection among gynecology clinic outpatients in Yunnan Province between October 2019 and August 2023. The primary goal of this study was to provide epidemiological data to identify HPV subtypes that are more likely to cause persistent infections and those that are easier to eradicate in the local region. Materials and Methods Study population Data was collected from women who visited the gynecological clinic of the First People's Hospital of Yunnan Province between October 2019 and August 2023 and were advised to undergo routine HPV testing. The inclusion criteria is as follows: (i) visited the hospital's gynecological clinic, (ii) supplied cervical brush samples for HPV DNA testing, and (iii) were 15 y of age or older. The exclusion criteria is as follows: (i) male sex, (ii) loss of pertinent clinical data, and (iii) age less than 15 y. The analysis of this database was approved by the Ethics Committee of the First People's Hospital of Yunnan Province (No. KHLL2023-KY068). The following variables were acquired: patient ID, date of HPV testing, age at HPV testing, and HPV type results. Data were de-identified before analysis. Details are presented in Fig. 1. Cervical sample collection Vaginal medication and flushing were prohibited for three days before to sampling, and vaginal intercourse was prohibited for 24 h before sampling. Using a cervical brush, exfoliated cervical cells were collected and kept in sterile sample tubes with cell preservation solution at 4℃ (HEALTH Gene Technologies Co., Ltd., Ningbo, China). DNA extraction DNA was extracted from the samples within 24 h of collection using a nucleic acid extraction kit (HEALTH Gene Technologies Co., Ltd., Ningbo, China) according to the manufacturer's instructions. Samples comprising exfoliated cervical cells in cell preservation solution were mixed with a vortex mixer, moved into a 1.5 ml sterile tube, and centrifuged for 5 min at 12,000 × g. After discarding the supernatant, 500 µL of PBS was used to wash the cell pellet and get rid of any contaminants, such as blood or mucus. Ultimately, the pellet was lysed for 15 min at 100 °C using 200 µL of 5% Chelex-100 chelating resin, and then centrifuged for 5 min at 12,000 g. HPV testing and genotyping HPV genotyping was performed in accordance with the manufacturer’s instructions using an HPV Genotyping Kit (HEALTH Gene Technologies Co., Ltd., Ningbo, China). Specific primers were created for the human β-globin locus, plasmid pcDNA 3.1(+), and early genes E6, E7, and E1 of the HPV genome[12]. PCR amplification was performed in a Veriti heat cycler (Applied Biosystems, Foster City, CA, USA) using the following program. The reaction mixture contained DNA template (9 µL), PCR Master Mix (9 µL), and Taq DNA polymerase (2 µL). 55 min at 42 °C, 8 min of pre-denaturation at 94 °C, 35 cycles of 94 °C for 30 s, 60 °C for 30 s, and 70 °C for 1 min, with a final 1-min extension step at 70 °C. PCR products were examined using a 3500DX Genetic Analyzer (Applied Biosystems, Foster City, CA, USA). Depending on the length of the PCR product, this analyzer could identify 25 HPV subtypes via capillary ectrophoresis in a single analysis. These subtypes include 15 HR-HPVs (16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 68, 73, and 82), 3 probable HR-HPVs (26, 53, and 66), and 7 LR-HPVs (6, 11, 42, 43, 44, 81, and 83). To ensure that insufficient sample was not the cause of the negative results, pcDNA and human β-globin amplicon production were carried out to track the PCR process. Statistical analysis To compute the incidence, persistence, and clearance rates, participants who were retested for HPV within 24 months of the initial test were included. The 24 months were divided into four calendar periods: within 6 months (0–6 months), 6–12 months (6–12 months), 12–18 months (12–18 months), and 12–24 months (18–24 months) following the initial test. The number of individuals who tested negative for HPV for the first time and underwent a follow-up test within two years served as the denominator for calculating the rate of incident infections, whereas the number of individuals who tested positive for any HPV subtype in their second test served as the numerator[13]. The HPV persistence rates were calculated using the number of individuals who tested positive for the first time and retested within two years as the denominator, and the number of individuals who tested positive a second time for the same HPV subtype as the numerator. The denominator of the HPV clearance rate was the number of individuals who tested positive for the first time and re-tested within 24 months, whereas the numerator was the number of individuals who tested negative for the second time for the same HPV type. The statistical software SPSS (version 26.0; SPSS Inc., Chicago, USA) was used for all statistical analyses. Statistical significance was set at P < 0.05. Results Overall characteristics of women with multiple HPV results among gynecological outpatients We enrolled 45,149 individuals who fulfilled the enrollment requirements to examine the prevalence of HPV infection in the study area. Of these, only 10.01% (N=4521) of individuals underwent two or more HPV tests in a 24-month period (Fig. 1). Of the individuals who underwent multiple HPV tests, 76.97% (N=3272) underwent two tests. The number of HPV tests per woman ranged from one to eight. The average age was 40.09±10.30 y. The groups were separated based on age as follows: 60 y. The proportion of individuals in these age categories was 15.86%, 34.97%, 30.55%, 15.00%, and 3.63%, respectively. 39.50 Of those who underwent retesting for HPV, 39.50% had a single infection and 16.55% had multiple infections (Table 1). 42.00 Of the individuals who tested positive for HPV, 42.00% were HR HPV carriers and 14.05% were LR HPV carriers (Table 1). Overall characteristics of HPV incidence Among women who underwent another HPV test during a 24-month period, the overall incidence rates of HPV, 2vHPV, 4vHPV, and 9vHPV were 36.84% (95% confidence interval: 34.72% - 38.96%), 4.43% (3.52% - 5.33%), 5.64% (4.62% -6.65%), and 18.42% (16.71% - 20.13%), respectively (Table 2). Age groups 30-39 and 40-49 accounted for the bulk of incident infections. The top five HPV subtypes by incidence frequency were 52, 51, 81, 58, and 16 (Fig. 2a). For HR-HPV, the incidence rates of the first three HPV subtypes were 5.59% (HPV 52), 3.72% (HPV 51), and 3.37% for (HPV 58), respectively. For the LR HPV, the incidence rate of the first three HPV subtypes was 3.47% (HPV 81), 2.67% (HPV 43), and 2.52% (HPV 42), respectively (Fig. 2a). Women who had another HPV test between 0–6, 6–12, 12–18, and 18–24 months after their first test had overall incidence rates of any kind of HPV of 13.14%, 15.60%, 8.76%, and 11.83%, respectively (Fig. 3). The most frequent subtypes of incident infections in the 0–6-and 6–12 month time intervals were HPV 52, 51, 58, and 53. Extended screening intervals were associated with higher incidence rates of HPV 16 and 39. Among all women retested at different intervals, the four most prevalent LR HPVs were HPV81, HPV42, HPV43, and HPV44. With longer retesting intervals, there was a progressive increase in the incidence of HPV 42, indicating that HPV42 may take a longer time to clear. Overall characteristics of HPV persistence The overall persistent rates of any HPV, 2vHPV, 4vHPV, and 9vHPV among women who had another HPV test during a 24-month period were 55.56% (95% confidential interval: 53.62%-57.50%), 7.10% (6.10%-8.10%), 7.93% (6.88%-8.98%), and 28.57% (26.81%-30.33%), respectively (Table 3). The proportions of persistent positive infections in age groups <30, 30-39, 40-49, 50-59, and ≥60 were 56.60%, 49.94%, 49.43%, 69.23%, and 78.99%, respectively. Age-related increases in persistent HPV infections have been considerable. According to the frequency of persistence, the top five HPV subtypes were 42, 52, 58, 81, and 56 (Fig. 1b). The first three HPV subtypes for HR HPV had persistence rates of 47.83% (HPV 52), 46.88% (HPV 58), and 41.18% (HPV 56). The first three HPV subtypes for LR HPV had persistence rates of 51.82% (HPV 42), 45.65% (HPV 81), and 32.93% (HPV 44) (Fig. 1b). Between 0–6, 6–12, 12–18, and 18–24 months after their initial test, women who underwent another HPV test showed persistence rates for all HPV types of 12.57%, 13.26%, 6.62%, and 6.37%, respectively (Fig. 4). It is evident from the time interval results that among the HR HPVs, persistent infections were longer for HPV 58 and 52. For LR HPV, HPV42 and 81 showed longer durations of persistent infection. Overall characteristics of HPV clearance Among women who underwent another HPV test within a 24-month period, the overall clearance rates for any HPV, 2vHPV, 4vHPV, and 9vHPV were 74.43%(95% confidential interval: 72.73%-76.13%), 13.46%(12.13%-14.79), 17.68%(16.19%-19.17%), and 44.44%(42.50%-46.37%), respectively (Table 4). In age groups <30, 30-39, 40-49, 50-59, and ≥60, the percentage of clearance rates among HPV positive individuals was 77.87%, 76.66%, 75.64%, 67.55%, and 62.18%, correspondingly. The HPV clearance rate decreased progressively with age. HPV 26, 83, 11, 82, and 44 were the top five HPV subtypes that were the most easily eradicated (Fig. 1b). The top three HR HPV subtypes with the lowest clearance rates were 58(53.66%), 52(53.99%), and 35(62.50%). HPV 42(56.93%), 81(62.50%), and 43(85.15%) were the three LR HPV subtypes with the lowest clearance rates. The majority of HPV infections cleared rapidly, with two-thirds cleared within a year (Fig. 5). Discussion The importance of persistent HPV infection in cervical cancer has been extensively acknowledged. Moreover, cervical cancer remains one of the most common cancers in women, despite the enormous efforts made in HPV vaccination programs. Therefore, there is an urgent need to develop efficient therapies for both HPV infections and HPV-associated disorders linked to HPV. To the best of our knowledge, this is the most recent report on the incidence of HPV infection in Yunnan in recent years. In this study, the overall incidence rates of HPV, 2vHPV, 4vHPV, and 9vHPV were 36.84%, 4.43%, 5.64%, and 18.42%, respectively. The age ranges–30-39 and 40-49 y had the highest incidence rates. HPV 52 was associated with the highest incidence of infection, followed by HPV 51, HPV 81, HPV 58, and HPV 16. The HPV subtypes with the highest incidence rates in Yunnan between 2012 and 2014 were HPV 16, 52, and 83[13], implying that with the introduction of the HPV vaccine, the subtypes of HPV that are most common locally are gradually changing. The overall incidence rates in our study were higher than those in women in Guangdong (10.58%) and in elderly women in Sweden (2.4%)[14]. In a different survey, young Dutch women aged 16–29 y had an overall HPV incidence of 45%[15]. Variations in the follow-up length, populations selected, timeframes, and other factors could all contribute to these variations in the rate of incident infections. The overall persistence rates of HPV, 2vHPV, 4vHPV, and 9vHPV in our study were 55.56%, 7.10%,7.93%, and 28.57%, respectively. The highest rates of persistent infection were found in the 59 age groups, HPV subtypes 42, 52, 58, 81, and 56 showed the highest rates of persistent infection, while both the LR HPV 42 and 81 and HR HPV 58 and 52 subtypes persisted longer than the other subtypes. In addition, there were significant changes in the subtypes of persistent infections from the 2012-2014 data. Between 2012 and 2014, patients with HPV 43 (16.7%),16 (15.3%), 58 (14.0%), 6 (12.2%), and 52 (8.5%) showed the highest rates of persistent infection [13]. The median HPV persistence rates at 12 and 24 months after therapy were reported to be 13% and 4%, respectively[16]. Compared to Daqing(34.12%)[17], Heilongjiang(33.9%)[18], Wuhan(46.51%)[19], Mexico(38.00%)[20], and the Netherlands(44.10%)[21], the persistent HPV infection rate in our study was higher. These disparities may be due to factors such as age, nation, race, socioeconomic status, and access to healthcare. The HPV persistence rate was 47.55% at 24 months, and the top three HPV subtypes of persistent infections were 42, 53, and 81 [6]. HPV 42 was more frequently persistent than other HPV types, which agrees with the findings from Guangdong[6]. Despite not being included in the vaccine, HPV subtype 42 has been found to be significantly associated with certain occurrences of cervical intraepithelial neoplasia (CIN)[22] and digital papillary adenocarcinoma (DPA)[23]. Future immunization programs should consider this subtype. The overall clearance rates of HPV, 2vHPV, 4vHPV, and 9vHPV in the present study were 74.43%, 13.46%,17.68%, and 44.44%, respectively. The clearance rate increases with age. The most probable HPV subtypes to be cleared were 26, 83, 11, 82, and 44, the least likely HR HPV subtypes were 58, 52, and 35, and the least likely to be cleared LR HPV subtypes were 42, 81, and 43. Among Colombian women, HPV-18 and HPV-31 subtypes have the lowest chances of being cleared[8]. The 24-month HPV clearance rate among women was 40.4% in Ouro Preto, Brazil [24] and 52.44% in Guangdong [6]. As reported by Tuerxun, among rural Uyghur women in China, the clearance rate of HPV infection was 59.74% at the 12-month follow-up and 69.13% at the 24-month follow-up [25]. The subtype of infection, viral load, person's location, and other factors can contribute to these variations. Apart from HPV 16 and 18, HPV 58 is the most commonly found HPV type in individuals with HSIL and is a critical risk factor for cervical disease progression[26-28]. As HPV58 is the most persistent and challenging virus to eradicate in Yunnan, it needs greater consideration, particularly for the older population. This study has certain limitations. First, the patient sample size was small; larger sample sizes are needed in future research to confirm our findings. As Yunnan is a multiethnic province, more accurate information can be obtained by studying a variety of centers and ethnic groups. Second, gynecological outpatients were the target population of the study, which may have contributed to the increased proportion of persistent infections in our population. Third, we were unable to include additional variables associated with HPV incidence, persistence, and clearance, such as geographic, sociodemographic, behavioral, cervical cytology, and histology results. In conclusion, Yunnan women had a higher likelihood of incident and persistent infections and a lower likelihood of HPV 58, 52, 42, and 81 clearance. Older adults are more prone to persistent HPV infection, whereas younger individuals are more likely to recover from it. Declarations Ethics approval and consent to participate As this study was a retrospective study and the identities of patients were intentionally anonymized, no individual informed consent was required. The analysis of this database was approved by the Ethics Committee of the First People's Hospital of Yunnan Province (No. KHLL2023-KY068). Consent for publication Not applicable. Availability of data and materials Data can be requested by the corresponding author. No datasets were generated or analysed during the current study. Competing Interests None to declare. The authors declare no competing interests. The authors have no relevant financial or non-financial interests to disclose. Funding This project was supported by Yunnan Provincial Key Laboratory of Clinical Virology(grant No. 202002AG070062), Research Fund for the Doctoral Program of the First People Hospital of Yunnan Province(grant No. KHBS-2020-009) and the National Natural Science Foundation of China(grant No.82060664). Authors’ Contribution Ya Xu designed the experiments and analyzed the data. Yafei Huang, Yan Guo, Ting Su and Qiuting Duan performed the experiments. Xin Fan, Yufan Zhang, Jinxiu Wan and Xiangcong Wei collected the clinical information. Guiqian Zhang and Yi Sun wrote the main manuscript text. All authors reviewed the manuscript and approved the manuscript and agree to be accountable for all aspects of the research in ensuring that the accuracy or integrity of any part of the work are appropriately investigated and resolved. Acknowledgements We appreciated the colleagues of the laboratory for collecting data. 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Front Oncol12:812076 Tables Table 1 Prevalence of HPV infection among women with multiple HPV results Characteristic ＜30 30-39 40-49 50-59 ≥60 Total (n) % HPV negative 247 754 679 262 45 1987 43.95% HPV positive 470 827 702 416 119 2534 56.05% Single infection 294 589 522 301 80 1786 39.50% Multiple infection 176 238 180 115 39 748 16.55% HR HPV 312 635 536 320 96 1899 42.00% LR HPV 158 192 166 96 23 635 14.05% Total 717 1581 1381 678 164 4521 100.00% Table 2 Type-specific HPV incidence among women who retested for the virus HPV subtypes ＜30 30-39 40-49 50-59 ≥60 Total Incidence Rates 95% CI Any HPV 119 235 202 138 38 732 36.84% 34.72% - 38.96% 2V HPV 13 28 23 17 7 88 4.43% 3.52% - 5.33% 4V HPV 17 35 32 21 7 112 5.64% 4.62% -6.65% 9VHPV 54 102 114 79 17 366 18.42% 16.71% - 20.13% Table 3 Type-specific HPV persistence among women who retested for the virus HPV subtypes ＜30 30-39 40-49 50-59 ≥60 Total Persistent Rates 95% CI Any HPV 266 413 347 288 94 1408 55.56% 53.62%-57.50% 2V HPV 35 67 41 27 10 180 7.10% 6.10%-8.10% 4V HPV 42 72 42 34 11 201 7.93% 6.88%-8.98% 9VHPV 149 217 178 138 42 724 28.57% 26.81%-30.33% Table 4 Type-specific HPV clearance among women who retested for the virus HPV subtypes ＜30 30-39 40-49 50-59 ≥60 Total Clearance Rates 95% CI Any HPV 366 634 531 281 74 1886 74.43% 72.73%-76.13% 2V HPV 73 103 89 56 20 341 13.46% 12.13%-14.79 4V HPV 120 134 108 63 23 448 17.68% 16.19%-19.17% 9VHPV 255 382 291 146 52 1126 44.44% 42.50%-46.37% Additional Declarations No competing interests reported. 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14:45:27","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4606669/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4606669/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":60600620,"identity":"a628e494-3b40-4860-a6b9-61a7f25e751c","added_by":"auto","created_at":"2024-07-18 16:02:16","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":84917,"visible":true,"origin":"","legend":"\u003cp\u003eFlow chart showing the inclusion and deletion of participants\u003c/p\u003e","description":"","filename":"Figure1.png","url":"https://assets-eu.researchsquare.com/files/rs-4606669/v1/c8d085d9110894ccf57928f3.png"},{"id":60600621,"identity":"449846e6-d659-4f51-815b-0bc783d39981","added_by":"auto","created_at":"2024-07-18 16:02:16","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":139827,"visible":true,"origin":"","legend":"\u003cp\u003eOverall HPV genotype distribution of (a)HPV incidence, (b)persistence and (c)clearance\u003c/p\u003e","description":"","filename":"Figure2.png","url":"https://assets-eu.researchsquare.com/files/rs-4606669/v1/9f187874e66a4ee1326ff9ff.png"},{"id":60602103,"identity":"fc924800-909f-4e0f-bcbb-2bf599f0d81e","added_by":"auto","created_at":"2024-07-18 16:10:16","extension":"png","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":351554,"visible":true,"origin":"","legend":"\u003cp\u003eOverall HPV genotype distribution of HPV incidence within 6 months (a), 6–12 months (b), 12–18 months (c), and 12–24 months (d)\u003c/p\u003e","description":"","filename":"Figure3.png","url":"https://assets-eu.researchsquare.com/files/rs-4606669/v1/46060a09e2024f9c689b8e4e.png"},{"id":60600624,"identity":"1c1d8e72-c180-47c2-aba1-f537a8239e0f","added_by":"auto","created_at":"2024-07-18 16:02:16","extension":"png","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":346965,"visible":true,"origin":"","legend":"\u003cp\u003eOverall HPV genotype distribution of HPV persistence within 6 months (a), 6–12 months (b), 12–18 months (c), and 12–24 months (d)\u003c/p\u003e","description":"","filename":"Figure4.png","url":"https://assets-eu.researchsquare.com/files/rs-4606669/v1/154b4508c69de6dc54919357.png"},{"id":60600623,"identity":"7086f3cc-73e7-4059-8a11-c14994f079c9","added_by":"auto","created_at":"2024-07-18 16:02:16","extension":"png","order_by":5,"title":"Figure 5","display":"","copyAsset":false,"role":"figure","size":67822,"visible":true,"origin":"","legend":"\u003cp\u003eOverall HPV genotype distribution of HPV clearance within 6 months, 6–12 months, 12–18 months, and 12–24 months\u003c/p\u003e","description":"","filename":"Figure5.png","url":"https://assets-eu.researchsquare.com/files/rs-4606669/v1/5318d1c05fb29487e0dd0e6a.png"},{"id":61101044,"identity":"a902240f-3960-41e2-ae63-614f6ef48fef","added_by":"auto","created_at":"2024-07-25 15:05:00","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1502346,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4606669/v1/db531ce4-0c4b-4d06-b7f7-270b7243e17f.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Incidence, persistence, and clearance of cervical Human Papillomavirus among gynecological outpatients in Kunming, Yunnan, China from 2019-2023: A retrospective cohort study","fulltext":[{"header":"Introduction","content":"\u003cp\u003eHuman papillomavirus (HPV) causes one of the most prevalent sexually transmitted diseases (STDs) worldwide, which is the HPV infection. According to numerous studies till date, HPV infection plays a central role in the occurrence of cervical cancer[1]. Despite the promotion of prophylactic vaccination, vaccination rates remain low, especially in underdeveloped countries. Moreover, only a few antiviral therapies are available for HPV infections, with its burden on public health increasing.\u003c/p\u003e \u003cp\u003eTo date, more than 200 HPV genotypes have been identified; based on their association with cancer, HPV has been categorized into high-risk HPV(HR-HPV) and low-risk HPV(LR-HPV) genotypes. In the majority of HPV-infected individuals, the infection is cleared by the immune system within 1 or 2 years of onset. However, a small number of infected people have a persistent or latent infection status for years, which contributes to malignant transformation. Persistent HPV infection plays an important role in the occurrence of cervical, anogenital, and head and neck cancers [2, 3]. According to several studies, the detection of the same carcinogenic HPV type over time may be particularly crucial for cervical carcinogenesis [4, 5].\u003c/p\u003e \u003cp\u003eRegional and population-specific differences are observed in the incidence, persistence, and clearance rates of HPV [6\u0026ndash;9]. In prepubertal girls and boys, HPV vaccination has proven to be highly successful in preventing HPV infection and associated illnesses with HPV infection [10]. Furthermore, China launched bivalent(2v), quadrivalent(4v), and nine-valent (9v) HPV vaccinations between July 2017 and the end of 2018[11]. Therefore, to better understand the local efficacy of HPV vaccination and provide a theoretical foundation for vaccination, a re-evaluation of the local rates of incidence, persistence, and clearance of HPV infections is required. The aim of the present study was to investigate the incidence, persistence, and clearance rates of HPV infection among gynecology clinic outpatients in Yunnan Province between October 2019 and August 2023. The primary goal of this study was to provide epidemiological data to identify HPV subtypes that are more likely to cause persistent infections and those that are easier to eradicate in the local region.\u003c/p\u003e"},{"header":"Materials and Methods","content":"\u003ch2\u003eStudy population\u003c/h2\u003e\n\u003cp\u003eData was collected from women who visited the gynecological clinic of the First People's Hospital of Yunnan Province between October 2019 and August 2023 and were advised to undergo routine HPV testing. The inclusion criteria is as follows: (i) visited the hospital's gynecological clinic, (ii) supplied cervical brush samples for HPV DNA testing, and (iii) were 15 y of age or older. The exclusion criteria is as follows: (i) male sex, (ii) loss of pertinent clinical data, and (iii) age less than 15 y. The analysis of this database was approved by the Ethics Committee of the First People's Hospital of Yunnan Province (No. KHLL2023-KY068). The following variables were acquired: patient ID, date of HPV testing, age at HPV testing, and HPV type results. Data were de-identified before analysis. Details are presented in Fig. 1.\u003c/p\u003e\n\u003ch2\u003eCervical sample collection\u003c/h2\u003e\n\u003cp\u003eVaginal medication and flushing were prohibited for three days before to sampling, and vaginal intercourse was prohibited for 24 h before sampling. Using a cervical brush, exfoliated cervical cells were collected and kept in sterile sample tubes with cell preservation solution at 4℃ (HEALTH Gene Technologies Co., Ltd., Ningbo, China).\u003c/p\u003e\n\u003ch2\u003eDNA extraction\u003c/h2\u003e\n\u003cp\u003eDNA was extracted from the samples within 24 h of collection using a nucleic acid extraction kit (HEALTH Gene Technologies Co., Ltd., Ningbo, China) according to the manufacturer's instructions. Samples comprising exfoliated cervical cells in cell preservation solution were mixed with a vortex mixer, moved into a 1.5 ml sterile tube, and centrifuged for 5 min at 12,000 × g. After discarding the supernatant, 500 µL of PBS was used to wash the cell pellet and get rid of any contaminants, such as blood or mucus. Ultimately, the pellet was lysed for 15 min at 100 °C using 200 µL of 5% Chelex-100 chelating resin, and then centrifuged for 5 min at 12,000 g.\u003c/p\u003e\n\u003ch2\u003eHPV testing and genotyping\u003c/h2\u003e\n\u003cp\u003eHPV genotyping was performed in accordance with the manufacturer’s instructions using an HPV Genotyping Kit (HEALTH Gene Technologies Co., Ltd., Ningbo, China). Specific primers were created for the human β-globin locus, plasmid pcDNA 3.1(+), and early genes E6, E7, and E1 of the HPV genome[12]. PCR amplification was performed in a Veriti heat cycler (Applied Biosystems, Foster City, CA, USA) using the following program. The reaction mixture contained DNA template (9 µL), PCR Master Mix (9 µL), and Taq DNA polymerase (2 µL). 55 min at 42 °C, 8 min of pre-denaturation at 94 °C, 35 cycles of 94 °C for 30 s, 60 °C for 30 s, and 70 °C for 1 min, with a final 1-min extension step at 70 °C. PCR products were examined using a 3500DX Genetic Analyzer (Applied Biosystems, Foster City, CA, USA). Depending on the length of the PCR product, this analyzer could identify 25 HPV subtypes via capillary ectrophoresis in a single analysis. These subtypes include 15 HR-HPVs (16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, 68, 73, and 82), 3 probable HR-HPVs (26, 53, and 66), and 7 LR-HPVs (6, 11, 42, 43, 44, 81, and 83). To ensure that insufficient sample was not the cause of the negative results, pcDNA and human β-globin amplicon production were carried out to track the PCR process.\u003c/p\u003e\n\u003ch2\u003eStatistical analysis\u003c/h2\u003e\n\u003cp\u003eTo compute the incidence, persistence, and clearance\u0026nbsp;rates, participants who were retested for HPV within 24 months of the initial test were included.\u0026nbsp;The 24 months were divided into four calendar periods: within 6 months (0–6\u0026nbsp;months), 6–12 months (6–12 months), 12–18 months (12–18 months), and 12–24 months (18–24 months) following the initial test.\u003c/p\u003e\n\u003cp\u003eThe number of individuals who tested negative for HPV for the first time and underwent a follow-up test within two years served as the denominator for calculating the rate of incident infections, whereas the number of individuals who tested positive for any HPV subtype in their second test served as the numerator[13].\u003c/p\u003e\n\u003cp\u003eThe HPV persistence rates were calculated using the number of individuals who tested positive\u0026nbsp;for the first time and retested within\u0026nbsp;two years as the denominator, and the number of individuals who tested positive a second time\u0026nbsp;for the same HPV subtype as the numerator.\u003c/p\u003e\n\u003cp\u003eThe denominator of the HPV clearance rate was the number of individuals who tested positive\u0026nbsp;for the first time and\u0026nbsp;re-tested within 24 months, whereas the numerator was the number of individuals who tested negative\u0026nbsp;for the second time\u0026nbsp;for the same HPV type.\u003c/p\u003e\n\u003cp\u003eThe statistical software SPSS (version 26.0; SPSS Inc., Chicago, USA) was used for all statistical analyses. Statistical significance was set at P \u0026lt; 0.05.\u003c/p\u003e"},{"header":"Results","content":"\u003ch2\u003eOverall characteristics of women with multiple HPV results among gynecological outpatients\u003c/h2\u003e\n\u003cp\u003eWe enrolled 45,149 individuals who fulfilled the enrollment requirements to examine the prevalence of HPV infection in the study area. Of these, only 10.01% (N=4521) of individuals underwent two or more HPV tests in a 24-month period (Fig. 1). Of the individuals who underwent multiple HPV tests, 76.97% (N=3272) underwent two tests. The number of HPV tests per woman ranged from one to eight. The average age was 40.09±10.30 y. The groups were separated based on age as follows: \u0026lt; 30, 30–39, 40–49, 50–59, and \u0026gt; 60 y. The proportion of individuals in these age categories was 15.86%, 34.97%, 30.55%, 15.00%, and 3.63%, respectively. 39.50 Of those who underwent retesting for HPV, 39.50% had a single infection and 16.55% had multiple infections (Table 1). 42.00 Of the individuals who tested positive for HPV, 42.00% were HR HPV carriers and 14.05% were LR HPV carriers (Table 1).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eOverall characteristics of HPV incidence\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eAmong women who underwent another HPV test during a 24-month period, the overall incidence rates of HPV, 2vHPV, 4vHPV, and 9vHPV were 36.84% (95% confidence interval: 34.72% - 38.96%), 4.43% (3.52% - 5.33%), 5.64% (4.62% -6.65%), and 18.42% (16.71% - 20.13%), respectively (Table 2). Age groups 30-39 and 40-49 accounted for the bulk of incident infections. The top five HPV subtypes by incidence frequency were 52, 51, 81, 58, and 16 (Fig. 2a). For HR-HPV, the incidence rates of the first three HPV subtypes were 5.59% (HPV 52), 3.72% (HPV 51), and 3.37% for (HPV 58), respectively. For the LR HPV, the incidence rate of the first three HPV subtypes was 3.47% (HPV 81), 2.67% (HPV 43), and 2.52% (HPV 42), respectively (Fig. 2a). Women who had another HPV test between 0–6, 6–12, 12–18, and 18–24 months after their first test had overall incidence rates of any kind of HPV of 13.14%, 15.60%, 8.76%, and 11.83%, respectively (Fig. 3). The most frequent subtypes of incident infections in the 0–6-and 6–12 month time intervals were HPV 52, 51, 58, and 53. Extended screening intervals were associated with higher incidence rates of HPV 16 and 39. Among all women retested at different intervals, the four most prevalent LR HPVs were HPV81, HPV42, HPV43, and HPV44. With longer retesting intervals, there was a progressive increase in the incidence of HPV 42, indicating that HPV42 may take a longer time to clear.\u003c/p\u003e\n\u003ch2\u003eOverall characteristics of HPV persistence\u003c/h2\u003e\n\u003cp\u003eThe overall persistent rates of any HPV, 2vHPV, 4vHPV, and 9vHPV among women who had another HPV test during a 24-month period were 55.56% (95% confidential interval: 53.62%-57.50%), 7.10% (6.10%-8.10%), 7.93% (6.88%-8.98%), and 28.57% (26.81%-30.33%), respectively (Table 3). The proportions of persistent positive infections in age groups \u0026lt;30, 30-39, 40-49, 50-59, and ≥60 were 56.60%, 49.94%, 49.43%, 69.23%, and 78.99%, respectively. Age-related increases in persistent HPV infections\u0026nbsp;have been considerable. According to\u0026nbsp;the frequency of persistence, the top five HPV subtypes were 42, 52, 58, 81, and 56 (Fig. 1b).\u0026nbsp;The first three HPV subtypes for HR HPV had persistence rates of 47.83% (HPV 52), 46.88% (HPV 58), and 41.18% (HPV 56). The first three HPV subtypes for LR HPV had persistence rates of 51.82% (HPV 42), 45.65% (HPV 81), and 32.93% (HPV 44) (Fig. 1b). Between 0–6, 6–12, 12–18, and 18–24 months after their initial test, women who underwent another HPV test showed persistence rates for all HPV types of 12.57%, 13.26%, 6.62%, and 6.37%, respectively (Fig. 4). It is evident from the time interval results that among\u0026nbsp;the HR HPVs, persistent infections were longer for HPV 58 and 52.\u0026nbsp;For LR HPV, HPV42 and 81 showed longer\u0026nbsp;durations of persistent infection.\u003c/p\u003e\n\u003ch2\u003eOverall characteristics of HPV clearance\u003c/h2\u003e\n\u003cp\u003eAmong women who underwent another HPV test within a 24-month period, the overall clearance rates for any HPV, 2vHPV, 4vHPV, and 9vHPV were 74.43%(95% confidential interval: 72.73%-76.13%), 13.46%(12.13%-14.79), 17.68%(16.19%-19.17%), and 44.44%(42.50%-46.37%), respectively (Table 4). In age groups \u0026lt;30, 30-39, 40-49, 50-59, and ≥60, the percentage of clearance rates among HPV positive individuals was 77.87%, 76.66%, 75.64%, 67.55%, and 62.18%, correspondingly. The HPV clearance rate decreased progressively with age. HPV 26, 83, 11, 82, and 44 were the top five HPV subtypes that were the most easily eradicated (Fig. 1b). The top three HR HPV subtypes with the lowest clearance rates were 58(53.66%), 52(53.99%), and 35(62.50%). HPV 42(56.93%), 81(62.50%), and 43(85.15%) were the three LR HPV subtypes with the lowest clearance rates. The majority of HPV infections cleared rapidly, with two-thirds cleared within a year (Fig. 5).\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eThe importance of persistent HPV infection in cervical cancer has been extensively acknowledged. Moreover, cervical cancer remains one of the most common cancers in women, despite the enormous efforts made in HPV vaccination programs. Therefore, there is an\u0026nbsp;urgent need to develop efficient therapies for both HPV infections and\u0026nbsp;HPV-associated disorders linked to HPV.\u0026nbsp;To the best of our knowledge, this is the most recent report on the incidence of HPV infection in Yunnan in recent years.\u003c/p\u003e\n\u003cp\u003eIn this study, the overall incidence rates of HPV, 2vHPV, 4vHPV, and 9vHPV were 36.84%, 4.43%, 5.64%, and 18.42%, respectively. The age ranges\u0026ndash;30-39 and 40-49 y had the highest incidence rates. HPV 52 was associated with the highest incidence\u0026nbsp;of infection, followed by\u0026nbsp;HPV 51, HPV 81, HPV 58, and HPV 16.\u0026nbsp;The HPV subtypes with the highest incidence rates in Yunnan between 2012 and 2014 were HPV 16, 52, and 83[13], implying that with the introduction of the HPV vaccine, the subtypes of HPV that are most common locally are gradually changing. The overall incidence rates in our study were higher than\u0026nbsp;those in women in Guangdong (10.58%) and\u0026nbsp;in elderly women in Sweden (2.4%)[14]. In a different survey,\u0026nbsp;young Dutch\u0026nbsp;women aged 16\u0026ndash;29\u0026nbsp;y had an overall HPV incidence of 45%[15]. Variations in the follow-up length, populations selected, timeframes, and other factors could all contribute to these variations in the rate of incident infections.\u003c/p\u003e\n\u003cp\u003eThe overall persistence rates of HPV, 2vHPV, 4vHPV, and 9vHPV in our study were 55.56%, 7.10%,7.93%, and 28.57%, respectively. The highest rates of persistent infection were found in the \u0026lt;30 and \u0026gt;59 age groups, HPV subtypes 42, 52, 58, 81, and 56 showed the highest rates of persistent infection, while both\u0026nbsp;the LR HPV 42 and 81 and HR HPV 58 and 52 subtypes persisted longer\u0026nbsp;than the other\u0026nbsp;subtypes.\u0026nbsp;In addition, there were significant changes in the subtypes of persistent infections from the 2012-2014 data. Between 2012 and 2014,\u0026nbsp;patients with HPV 43 (16.7%),16 (15.3%), 58 (14.0%), 6 (12.2%), and 52 (8.5%)\u0026nbsp;showed the highest rates of persistent infection\u0026nbsp;[13]. The median HPV persistence\u0026nbsp;rates at 12 and 24 months\u0026nbsp;after therapy were reported to be 13% and 4%, respectively[16]. Compared to Daqing(34.12%)[17], Heilongjiang(33.9%)[18], Wuhan(46.51%)[19], Mexico(38.00%)[20], and the Netherlands(44.10%)[21], the persistent HPV infection rate in our study was higher. These disparities may be due to factors such as age, nation, race, socioeconomic status,\u0026nbsp;and access to healthcare. The HPV persistence rate was 47.55% at 24 months,\u0026nbsp;and the top three HPV subtypes of persistent infections were 42, 53, and 81\u0026nbsp;[6]. HPV 42 was more frequently persistent than other HPV types, which agrees with the findings from Guangdong[6]. Despite not being included in the vaccine, HPV subtype 42 has been found to be significantly associated with certain occurrences of cervical intraepithelial neoplasia (CIN)[22]\u0026nbsp;and digital papillary adenocarcinoma (DPA)[23]. Future immunization programs should consider this subtype.\u003c/p\u003e\n\u003cp\u003eThe overall clearance rates of HPV, 2vHPV, 4vHPV, and 9vHPV in the present study were 74.43%, 13.46%,17.68%, and 44.44%, respectively. The clearance rate increases with age. The most probable\u0026nbsp;HPV subtypes\u0026nbsp;to be cleared were 26, 83, 11, 82, and 44, the least likely HR HPV subtypes were 58, 52, and 35,\u0026nbsp;and the least likely to be cleared LR HPV subtypes\u0026nbsp;were 42, 81, and 43. Among Colombian women, HPV-18 and HPV-31 subtypes have the lowest chances of being cleared[8]. The 24-month HPV clearance rate among women was 40.4% in Ouro Preto, Brazil\u0026nbsp;[24]\u0026nbsp;and 52.44% in Guangdong\u0026nbsp;[6]. As reported by Tuerxun, among rural Uyghur women in China, the clearance rate of HPV infection was 59.74% at the 12-month follow-up and 69.13% at the 24-month follow-up\u0026nbsp;[25]. The subtype of infection, viral load, person\u0026apos;s location, and other factors can contribute to these variations. Apart from HPV 16 and 18, HPV 58 is the most commonly found HPV type in individuals with HSIL and is\u0026nbsp;a critical risk factor for cervical disease progression[26-28]. As HPV58 is the most persistent and challenging\u0026nbsp;virus to eradicate in Yunnan, it needs greater\u0026nbsp;consideration, particularly for the older population.\u003c/p\u003e\n\u003cp\u003eThis study has certain limitations. First, the patient sample size was small; larger sample sizes are needed in future research to confirm our findings. As Yunnan is a multiethnic province, more accurate information can be obtained by studying a variety of centers and ethnic groups. Second, gynecological outpatients were the\u0026nbsp;target population\u0026nbsp;of the study, which\u0026nbsp;may have contributed to the increased proportion of persistent infections in our population. Third, we were unable to include additional variables associated with HPV incidence, persistence, and clearance, such as geographic, sociodemographic, behavioral, cervical cytology, and histology results.\u003c/p\u003e\n\u003cp\u003eIn conclusion, Yunnan women had a higher likelihood of incident and persistent infections and a lower likelihood of HPV 58, 52, 42, and 81 clearance. Older adults are more prone to persistent HPV infection, whereas younger individuals are more likely to recover from it.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003eEthics approval and consent to participate\u003c/p\u003e\n\u003cp\u003e\u0026nbsp;As this study was a retrospective study and the identities of patients were intentionally anonymized, no individual informed consent was required.\u0026nbsp;The analysis of this database was approved by the Ethics Committee of the First People\u0026apos;s Hospital of Yunnan Province (No. KHLL2023-KY068).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConsent for publication\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAvailability of data and materials\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eData can be requested by the corresponding author.\u0026nbsp;No datasets were generated or analysed during the current study.\u003c/p\u003e\n\u003cp\u003eCompeting Interests\u0026nbsp;\u003c/p\u003e\n\u003cp\u003eNone to declare. The authors declare no competing interests. The authors have no relevant financial or non-financial interests to disclose.\u003c/p\u003e\n\u003cp\u003eFunding\u003c/p\u003e\n\u003cp\u003eThis project was supported by Yunnan Provincial Key Laboratory of Clinical Virology(grant No. 202002AG070062), Research Fund for the Doctoral Program of the First People Hospital of Yunnan Province(grant No. KHBS-2020-009) and the National Natural Science Foundation of China(grant No.82060664).\u003c/p\u003e\n\u003cp\u003eAuthors\u0026rsquo; Contribution\u003c/p\u003e\n\u003cp\u003eYa Xu designed the experiments and analyzed the data. Yafei Huang,\u0026nbsp;Yan Guo,\u0026nbsp;Ting Su and Qiuting Duan performed the experiments. Xin Fan, Yufan Zhang, Jinxiu Wan and Xiangcong Wei collected the clinical information. Guiqian Zhang and Yi Sun wrote the main manuscript text. All authors reviewed the manuscript and approved the manuscript and agree to be accountable for all aspects of the research in ensuring that the accuracy or integrity of any part of the work are appropriately investigated and resolved.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAcknowledgements\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eWe appreciated the colleagues of the laboratory for collecting data.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eJain M, Yadav D, Jarouliya U, Chavda V, Yadav AK, Chaurasia B, Song M(2023)Epidemiology, Molecular Pathogenesis, Immuno-Pathogenesis, Immune Escape Mechanisms and Vaccine Evaluation for HPV-Associated Carcinogenesis. Pathogens12(12)\u003c/li\u003e\n\u003cli\u003eHo GY, Bierman R, Beardsley L, Chang CJ, Burk RD(1998)Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med338(7):423-8\u003c/li\u003e\n\u003cli\u003eRadley D, Saah A, Stanley M(2016)Persistent infection with human papillomavirus 16 or 18 is strongly linked with high-grade cervical disease. Hum Vaccin Immunother12(3):768-72\u003c/li\u003e\n\u003cli\u003eGillison ML, Koch WM, Capone RB, Spafford M, Westra WH, Wu L, Zahurak ML, Daniel RW, Viglione M, Symer DE, Shah KV, Sidransky D(2000)Evidence for a causal association between human papillomavirus and a subset of head and neck cancers. J Natl Cancer Inst92(9):709-20\u003c/li\u003e\n\u003cli\u003eSchiffman M, Herrero R, Desalle R, Hildesheim A, Wacholder S, Rodriguez AC, Bratti MC, Sherman ME, Morales J, Guillen D, Alfaro M, Hutchinson M, Wright TC, Solomon D, Chen Z, Schussler J, Castle PE, Burk RD(2005)The carcinogenicity of human papillomavirus types reflects viral evolution. Virology337(1):76-84\u003c/li\u003e\n\u003cli\u003eWallin KL, Wiklund F, Angstrom T, Bergman F, Stendahl U, Wadell G, Hallmans G, Dillner J(1999)Type-specific persistence of human papillomavirus DNA before the development of invasive cervical cancer. N Engl J Med341(22):1633-8\u003c/li\u003e\n\u003cli\u003eLi M, Liu T, Luo G, Sun X, Hu G, Lu Y, R HX, Zou H, Luo X(2021)Incidence, persistence and clearance of cervical human papillomavirus among women in Guangdong, China 2007-2018: A retrospective cohort study. J Infect Public Health14(1):42-9\u003c/li\u003e\n\u003cli\u003eZhou Y, Zhou X, Lin YF, Luo G, Lu Y, Wang Z, Li P, Luo Z, Meng X, Tian T, Fu L, Dai J, Zou H(2022)Incidence, Persistence, and Clearance of Anal Human Papillomavirus among Men Who Have Sex with Men in China: An Observational Cohort Study. Pathogens11(3)\u003c/li\u003e\n\u003cli\u003eSoto-De Leon SC, Del Rio-Ospina L, Camargo M, Sanchez R, Moreno-Perez DA, Perez-Prados A, Patarroyo ME, Patarroyo MA(2014)Persistence, clearance and reinfection regarding six high risk human papillomavirus types in Colombian women: a follow-up study. BMC Infect Dis14:395\u003c/li\u003e\n\u003cli\u003eKoshiol J, Lindsay L, Pimenta JM, Poole C, Jenkins D, Smith JS(2008)Persistent human papillomavirus infection and cervical neoplasia: a systematic review and meta-analysis. Am J Epidemiol168(2):123-37\u003c/li\u003e\n\u003cli\u003ePaavonen J, Naud P, Salmeron J, Wheeler CM, Chow SN, Apter D, Kitchener H, Castellsague X, Teixeira JC, Skinner SR, Hedrick J, Jaisamrarn U, Limson G, Garland S, Szarewski A, Romanowski B, Aoki FY, Schwarz TF, Poppe WA, Bosch FX, Jenkins D, Hardt K, Zahaf T, Descamps D, Struyf F, Lehtinen M, Dubin G, Group HPS(2009)Efficacy of human papillomavirus (HPV)-16/18 AS04-adjuvanted vaccine against cervical infection and precancer caused by oncogenic HPV types (PATRICIA): final analysis of a double-blind, randomised study in young women. Lancet374(9686):301-14\u003c/li\u003e\n\u003cli\u003eYin Y(2017)HPV vaccination in China needs to be more cost-effective. Lancet390(10104):1735-6\u003c/li\u003e\n\u003cli\u003eZou H, Sun Y, Zhang G, Tu Y, Meng X, Liu T, Ping Z, Fan X, Gao Y(2016)Positivity and incidence of human papillomavirus in women attending gynecological department of a major comprehensive hospital in Kunming, China 2012-2014. J Med Virol88(4):703-11\u003c/li\u003e\n\u003cli\u003eLanner L, Lindstrom AK(2020)Incidence of HPV and HPV related dysplasia in elderly women in Sweden. PLoS One15(3):e0229758\u003c/li\u003e\n\u003cli\u003eMollers M, Boot Hein J, Vriend Henrike J, King Audrey J, van den Broek Ingrid VF, van Bergen Jan EA, Brink Antoinette AT, Wolffs Petra FG, Hoebe Christian JP, Meijer Chris JL, van der Sande Marianne AB, de Melker Hester E(2013)Prevalence, incidence and persistence of genital HPV infections in a large cohort of sexually active young women in the Netherlands. Vaccine31(2):394-401\u003c/li\u003e\n\u003cli\u003eHoffman SR, Le T, Lockhart A, Sanusi A, Dal Santo L, Davis M, McKinney DA, Brown M, Poole C, Willame C, Smith JS(2017)Patterns of persistent HPV infection after treatment for cervical intraepithelial neoplasia (CIN): A systematic review. Int J Cancer141(1):8-23\u003c/li\u003e\n\u003cli\u003eLi N, Hang D, Yang L, Feng X, Lyu Z, Xie S, Zhou J, Wu L, Li X, Li N, Cheng M, Zhang K, Zhang Z, Cui H, Yin J, Hu Z, Shen H, Dai M(2017)Persistence of type-specific human papillomavirus infection among Daqing City women in China with normal cytology: a pilot prospective study. Oncotarget8(46):81455-61\u003c/li\u003e\n\u003cli\u003eLiu J, Shi Y, Wang L, Wang J, Fan D, Han S, Wei L(2020)Epidemiology and persistence of cervical human papillomavirus infection among outpatient women in Heilongjiang province: A retrospective cohort study. J Med Virol92(12):3784-92\u003c/li\u003e\n\u003cli\u003ePan S, Wei W, Du X, Li Z, Tuo J, Zhang M, Liu Q(2022)Factors associated with persistence and clearance of HPV16/18 among rural Chinese women: a cohort study in Wufeng, Hubei province. Women Health62(4):276-86\u003c/li\u003e\n\u003cli\u003eOyervides-Munoz MA, Perez-Maya AA, Sanchez-Dominguez CN, Berlanga-Garza A, Antonio-Macedo M, Valdez-Chapa LD, Cerda-Flores RM, Trevino V, Barrera-Saldana HA, Garza-Rodriguez ML(2020)Multiple HPV Infections and Viral Load Association in Persistent Cervical Lesions in Mexican Women. Viruses12(4)\u003c/li\u003e\n\u003cli\u003evan der Weele P, van Logchem E, Wolffs P, van den Broek I, Feltkamp M, de Melker H, Meijer CJ, Boot H, King AJ(2016)Correlation between viral load, multiplicity of infection, and persistence of HPV16 and HPV18 infection in a Dutch cohort of young women. J Clin Virol83:6-11\u003c/li\u003e\n\u003cli\u003eRegauer S, Reich O, Kashofer K(2019)Thin variant of high-grade squamous intraepithelial lesion - relationship with high-risk and possibly carcinogenic human papilloma virus subtypes and somatic cancer gene mutations. Histopathology75(3):405-12\u003c/li\u003e\n\u003cli\u003eLeiendecker L, Neumann T, Jung PS, Cronin SM, Steinacker TL, Schleiffer A, Schutzbier M, Mechtler K, Kervarrec T, Laurent E, Bachiri K, Coyaud E, Murali R, Busam KJ, Itzinger-Monshi B, Kirnbauer R, Cerroni L, Calonje E, Rutten A, Stubenrauch F, Griewank KG, Wiesner T, Obenauf AC(2023)Human Papillomavirus 42 Drives Digital Papillary Adenocarcinoma and Elicits a Germ Cell-like Program Conserved in HPV-Positive Cancers. Cancer Discov13(1):70-84\u003c/li\u003e\n\u003cli\u003eMiranda PM, Silva NN, Pitol BC, Silva ID, Lima-Filho JL, Carvalho RF, Stocco RC, Becak W, Lima AA(2013)Persistence or clearance of human papillomavirus infections in women in Ouro Preto, Brazil. Biomed Res Int2013:578276\u003c/li\u003e\n\u003cli\u003eTuerxun G, Abudurexiti G, Abulizi G(2023)Prevalence, persistence, clearance and risk factors for HPV infection in rural Uyghur women in China. BMC Womens Health23(1):433\u003c/li\u003e\n\u003cli\u003eSeong J, Ryou S, Lee J, Yoo M, Hur S, Choi BS, Korea HPVCS(2021)Enhanced disease progression due to persistent HPV-16/58 infections in Korean women: a systematic review and the Korea HPV cohort study. Virol J18(1):188\u003c/li\u003e\n\u003cli\u003eSong JS, Kim EJ, Choi J, Gong G, Sung CO(2013)Significance of HPV-58 infection in women who are HPV-positive, cytology-negative and living in a country with a high prevalence of HPV-58 infection. PLoS One8(3):e58678\u003c/li\u003e\n\u003cli\u003eYi B, Xu Q, Zhang Z, Zhang J, Xu Y, Huang L, Hu Y, Tu Q, Chen J(2022)Implications of Persistent HPV52 and HPV58 Positivity for the Management of Cervical Lesions. Front Oncol12:812076\u003c/li\u003e\n\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTable 1 Prevalence of HPV infection among women with multiple HPV results\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd width=\"21.541155866900176%\"\u003e\n \u003cp\u003eCharacteristic\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e＜30\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e30-39\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e40-49\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e50-59\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e\u0026ge;60\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003eTotal (n)\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"21.541155866900176%\"\u003e\n \u003cp\u003eHPV negative\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e247\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e754\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e679\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e262\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e45\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e1987\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e43.95%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"21.541155866900176%\"\u003e\n \u003cp\u003eHPV positive\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e470\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e827\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e702\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e416\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e119\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e2534\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e56.05%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"21.541155866900176%\"\u003e\n \u003cp\u003eSingle infection\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e294\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e589\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e522\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e301\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e80\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e1786\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e39.50%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"21.541155866900176%\"\u003e\n \u003cp\u003eMultiple infection\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e176\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e238\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e180\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e115\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e39\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e748\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e16.55%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"21.541155866900176%\"\u003e\n \u003cp\u003eHR HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e312\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e635\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e536\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e320\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e96\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e1899\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e42.00%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"21.541155866900176%\"\u003e\n \u003cp\u003eLR HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e158\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e192\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e166\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e96\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e23\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e635\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e14.05%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"21.541155866900176%\"\u003e\n \u003cp\u003eTotal\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e717\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e1581\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e1381\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e678\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e164\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e4521\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"11.208406304728546%\"\u003e\n \u003cp\u003e100.00%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eTable 2 Type-specific HPV incidence among women\u0026nbsp;who retested for the virus\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\" width=\"592\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\"\u003e\n \u003cp\u003eHPV subtypes\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e＜30\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e30-39\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e40-49\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e50-59\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e\u0026ge;60\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003eTotal\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\"\u003e\n \u003cp\u003eIncidence Rates\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\"\u003e\n \u003cp\u003e95% CI\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\"\u003e\n \u003cp\u003eAny HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"bottom\"\u003e\n \u003cp\u003e119\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"bottom\"\u003e\n \u003cp\u003e235\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"bottom\"\u003e\n \u003cp\u003e202\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"bottom\"\u003e\n \u003cp\u003e138\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"bottom\"\u003e\n \u003cp\u003e38\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"bottom\"\u003e\n \u003cp\u003e732\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\" valign=\"top\"\u003e\n \u003cp\u003e36.84%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e34.72% - 38.96%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e2V HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e13\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e28\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e23\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e17\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e7\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e88\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\" valign=\"top\"\u003e\n \u003cp\u003e4.43%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e3.52% - 5.33%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e4V HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e17\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e35\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e32\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e21\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e7\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e112\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\" valign=\"top\"\u003e\n \u003cp\u003e5.64%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e4.62% -6.65%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e9VHPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e54\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e102\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e114\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e79\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e17\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e366\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\" valign=\"top\"\u003e\n \u003cp\u003e18.42%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e16.71% - 20.13%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eTable 3 Type-specific HPV persistence among women\u0026nbsp;who retested for the virus\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\" width=\"592\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\"\u003e\n \u003cp\u003eHPV subtypes\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e＜30\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e30-39\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e40-49\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e50-59\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e\u0026ge;60\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003eTotal\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\"\u003e\n \u003cp\u003ePersistent Rates\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\"\u003e\n \u003cp\u003e95% CI\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\"\u003e\n \u003cp\u003eAny HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e266\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e413\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e347\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e288\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e94\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e1408\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\" valign=\"top\"\u003e\n \u003cp\u003e55.56%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e53.62%-57.50%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e2V HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e35\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e67\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e41\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e27\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e10\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e180\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\" valign=\"top\"\u003e\n \u003cp\u003e7.10%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e6.10%-8.10%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e4V HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e42\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e72\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e42\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e34\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e11\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e201\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\" valign=\"top\"\u003e\n \u003cp\u003e7.93%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e6.88%-8.98%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e9VHPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e149\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e217\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e178\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e138\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e42\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e724\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\" valign=\"top\"\u003e\n \u003cp\u003e28.57%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e26.81%-30.33%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e\n\u003cp\u003e\u003cstrong\u003e\u0026nbsp;\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eTable 4 Type-specific HPV clearance among women\u0026nbsp;who retested for the virus\u003c/p\u003e\n\u003ctable border=\"1\" cellspacing=\"0\" cellpadding=\"0\" width=\"592\"\u003e\n \u003ctbody\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\"\u003e\n \u003cp\u003eHPV subtypes\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e＜30\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e30-39\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e40-49\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e50-59\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003e\u0026ge;60\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\"\u003e\n \u003cp\u003eTotal\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\"\u003e\n \u003cp\u003eClearance Rates\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\"\u003e\n \u003cp\u003e95% CI\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\"\u003e\n \u003cp\u003eAny HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e366\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e634\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e531\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e281\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e74\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e1886\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\"\u003e\n \u003cp\u003e74.43%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e72.73%-76.13%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e2V HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e73\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e103\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e89\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e56\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e20\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e341\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\"\u003e\n \u003cp\u003e13.46%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e12.13%-14.79\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e4V HPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e120\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e134\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e108\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e63\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e23\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e448\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\"\u003e\n \u003cp\u003e17.68%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e16.19%-19.17%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003ctr\u003e\n \u003ctd width=\"12.66891891891892%\" valign=\"top\"\u003e\n \u003cp\u003e9VHPV\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e255\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e382\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e291\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e146\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e52\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"8.277027027027026%\" valign=\"top\"\u003e\n \u003cp\u003e1126\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"17.56756756756757%\"\u003e\n \u003cp\u003e44.44%\u003c/p\u003e\n \u003c/td\u003e\n \u003ctd width=\"20.10135135135135%\" valign=\"top\"\u003e\n \u003cp\u003e42.50%-46.37%\u003c/p\u003e\n \u003c/td\u003e\n \u003c/tr\u003e\n \u003c/tbody\u003e\n\u003c/table\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Human Papillomavirus, Incidence, Persistence, Clearance, Yunnan","lastPublishedDoi":"10.21203/rs.3.rs-4606669/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4606669/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003ch2\u003ePurpose\u003c/h2\u003e \u003cp\u003eHuman papillomavirus (HPV) infection is the primary driver of cervical cancer development and progression. This study aimed to determine the incidence, persistence, and clearance of type-specific HPV infections in Yunnan.\u003c/p\u003e\u003ch2\u003eMethods\u003c/h2\u003e \u003cp\u003eA retrospective cohort study was conducted between October 2019 and August 2023 on female gynecological outpatients residing in Yunnan, Southwest China. HPV genotyping was performed using a multiplex polymerase chain reaction and capillary electrophoresis. We investigated the incidence, persistence, and clearance of HPV in women who tested again at various times following the initial test.\u003c/p\u003e\u003ch2\u003eResults\u003c/h2\u003e \u003cp\u003eThis study included 45,149 participants; overall incidence of HPV infection was 36.84% with HPV 52 having the highest incidence, followed by HPV 51, 81, 58, and 16. The age ranges\u0026ndash;30\u0026ndash;39 and 40\u0026ndash;49 y had the highest incidence rates. The overall persistence rate of the HPV infection was 55.56%, while HPV subtypes 42, 52, 58, 81, and 56 showed the highest rates of persistent infection. The highest rates of persistent infection were found in the \u0026lt;\u0026thinsp;30 and \u0026gt;\u0026thinsp;59 y age groups. The overall HPV clearance rate was 74.43%, and it increased with age. The most probable HPV subtypes to be cleared were 26, 83, 11, 82, and 44, least likely HR HPV subtypes were 58, 52, and 35, and least likely LR HPV subtypes were 42, 81, and 43.\u003c/p\u003e\u003ch2\u003eConclusions\u003c/h2\u003e \u003cp\u003eWomen in Yunnan had a higher likelihood of incident and persistent infections and a lower likelihood of being cleared of HPV 58, 52, 42, and 81. Older adults are more prone to persistent HPV infection, whereas younger individuals are more likely to recover from infection.\u003c/p\u003e","manuscriptTitle":"Incidence, persistence, and clearance of cervical Human Papillomavirus among gynecological outpatients in Kunming, Yunnan, China from 2019-2023: A retrospective cohort study","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-07-18 16:02:11","doi":"10.21203/rs.3.rs-4606669/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"638a3a13-7e92-48a1-af19-756be664cbb9","owner":[],"postedDate":"July 18th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-07-25T14:56:52+00:00","versionOfRecord":[],"versionCreatedAt":"2024-07-18 16:02:11","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-4606669","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4606669","identity":"rs-4606669","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}