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Characteristics of Human Papillomavirus Infection Among Li et al. Virol J (2021) 18:51 https://doi.org/10.1186/s12985-021-01518-y RESEARCH Open Access Characteristics of human papillomavirus infection among women with cervical cytological abnormalities in the Zhoupu District, Shanghai City, China, 2014–2019 Ping Li1†, Qing Liu2†, Wei Li3, Zhou Liu5, Baoling Xing5, Suqin Wu5, Zhaoli Zhou1, Liping Sun1, He Ren1, Hengfeng Li4 and Huaping Li5* Abstract Background: Human papillomavirus (HPV) infection is currently the main cause of cervical cancer and precancerous lesions in female patients. By analyzing 6-year patient data from Shanghai Zhoupu Hospital in China, we retrospec- tively analyzed the epidemiological characteristics of women to determine the relationship between HPV genotype and cytological test results. Methods: From 2014 to 2019, 23,724 cases of cervical shedding were collected from Zhoupu Hospital in Shanghai, China. By comparing the results of HPV and ThinPrep cytology test (TCT), the HPV infection rate of patients was retro- spectively analyzed. HPV genotyping using commercial kits can detect 21 HPV subtypes (15 high-risk and 6 low-risk). According to the defnition of the Bethesda system, seven types of cervical cytology results were involved. Results: 3816 among 23,724 women, nearly 16.08%, were infected with HPV. The top three highest HPV prevalence rates were high-risk type infection, including HPV52 (3.19%), 58 (2.47%) and 16 (2.34%). The number of single-type HPV infections (3480 (91.20%)) was much larger than the number of multi-type ones (336 (8.8%)). Single-type infec- tions were mainly in women aged 50–60 (16.63%) and women under 30 (15.37%), while multi-type infections were more common in women over 60 (2.67%). By analyzing the long-term trends, between 2014 and 2019, HPV52, 58, and 16 subtypes changed signifcantly, and the HPV positive rate also changed signifcantly during this period. Among 4502 TCT positive women, 15 (4.04%), 125 (2.64%),159 (1.54%), 4202 (17.71%) and 1 (0.004%) had atypical glandular cells (AGC), high-grade squamous intraepithelial lesions (HSIL), low-grade squamous intraepithelial lesions (LSIL), atypical squamous cells (ASC)and cervical adenocarcinoma, respectively. The HPV infection rates were 66.08%, 63.99%, 115.20%, 119.50%, and 31.72% for NILM, AGCs, HSILs LSILs and ASCs, respectively. Conclusions: HPV and TCT screening were very important steps in the secondary prevention of cervical cancer. Through the tracking and analysis of HPV and TCT results in this study, it can provide valuable information for Shang- hai’s HPV screening and prevention strategies, and provide references for clinical decision-making in the treatment of cervical cancer and precancerous lesions. *Correspondence: [email protected] †Ping Li and Qing Liu contributed equally to this work 5 Shanghai University of Medicine and Health Sciences Afliated Zhoupu Hospital, Shanghai, China Full list of author information is available at the end of the article © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Li et al. Virol J (2021) 18:51 Page 2 of 11 Keywords: Epidemiological characteristic, Trend, China, Human papillomavirus, Genotype, ThinPrep cytological test Background and screening of cervical cancer. Terefore, this study Cervical cancer is the fourth largest cancer prevalence analyzed the epidemiological characteristics and long- among women in the world More than one-third of cer- term trends of HPV infection subtypes in Zhoupu Dis- vical cancers worldwide occur in China and India. Tere trict, Shanghai, especially for patients with abnormal are 106,000 cases of cervical cancer and 48,000 deaths in cytological examination results. Analyzing the relation- China [1], and the female cancer prevalence and mor- ship between HPV genotypes and cytological examina- tality are seventh and ninth respectively [2, 3]. Shanghai tion results will help the data of the specifc prevalence of is one of the largest cities in China. As the largest one HPV genotypes in Shanghai to encourage the implemen- among the 16 districts in Shanghai, the permanent pop- tation of HPV vaccine programs. ulation of Pudong New Area is approximately 5 million (approximately 20% of the total population of Shanghai). Methods From 2002 to 2015, the incidence of cervical cancer in Data source the urban and rural areas of Pudong New Area increased We collected the cervical exfoliations data of 23,724 by 9.8 and 15.5% each year. Te HPV infection rate and women who visited Shanghai Zhoupu hospital and the genotype distribution of Shanghai China have been received both TinPrep cytology test (TCT) and HPV statistics, not only in the Minhang district [4] but also in detection between 2014 and 2019. the Songjiang for both females [5] and males [6]. Located in the suburbs of Pudong New Area, research on the pre- Ethics statement vention and screening of cervical cancer in the Zhoupu Te study was approved by the Institutional Medical Eth- area is very meaningful [7]. ics Review Committee of Shanghai Zhoupu Hospital. Persistent human papillomavirus (HPV) infection will All 23,724 patients have signed informed consent. For cause cervical cancer [1] and cervical intraepithelial neo- patients younger than 18 years, their parents have signed plasia (CIN). According to the degree of afected epithe- a consent form. Confdentiality was ensured during lial tissue, CIN is graded according to grades 1–3, and the data collection process and the data were analyzed CIN3 is the most abnormal grade. In this study, CIN1 is anonymously. equivalent to low-grade squamous intraepithelial neo- Cytology testing plasia (LSIL), and ≥ CIN2 is equivalent to precancerous lesions or high-grade squamous intraepithelial neoplasia During non-menstrual periods, samples of cervical exfo- (HSIL). Patients with high-risk human papillomavirus liation were collected. Experienced Cytology experts in (HR-HPV) infection usually have multiple sexual part- gynecology conducted cytology based on cervical fuid. ners, which is positively correlated with cervical cancer According to the defnition by the Bethesda system, liq- [8, 9], LSIL, and HSIL infection. uid-based cytological terminality includes intraepithelial Our previous study confrmed that the HPV infec- lesions or malignant tumors (NILM), Low-grade squa- tion rate in Zhoupu district was 17.92% (10,670/59,541), mous intraepithelial lesion (LSIL) and high-squamous of which 86.81% (9263/10,670) was caused by HR-HPV. intraepithelial lesion (HSIL), atypical squamous cells of Te six HR-HPV genotypes with the highest positive rate undetermined signifcance (ASC-US), atypical squamous were HPV 52, 16, 58, 53, 39 and 51 [10]. Te distribution cells (ASC-H) which HSIL cannot be excluded, atypical of HPV genotypes was diferent in diferent regions and glandular cells (AGC), and adenocarcinoma. countries, which had led to geographic changes in the incidence and mortality of cervical cancer [11]. HPV genotyping Primary prevention (preventive HPV vaccination) and HPV typing test kits (Certifcate No. of China Food and secondary prevention (combined with efective HPV Drug Administration (2014): 3,402,188), using PCR testing and screening to treat cervical precancerous membrane hybridization, perform HPV genotyping on lesions) are very efective [1]. At present, in resource-rich collected samples. countries, the incidence of cervical cancer didn’t con- PCR membrane hybridization can detect 21 HPV gen- tinue to increase after the age of 40, which may well indi- otypes (15 h: 16, 18, 31, 33, 35, 39, 45, 51, 52, 56, 58, 59, cate that cancer can be prevented through screening [1]. 66, 68 and 6 LR: 6, 11, 42, 43 44 and 81), through reverse As one of the largest developing countries in the world, dot hybridization and envelope specifc probe membrane China needs to make further advances in the prevention for hybridization. Li et al. Virol J (2021) 18:51 Page 3 of 11 Statistical analysis All HPV and TCT data from 2014 to 2019 were com- bined into an Excel spreadsheet and then analyzed and plotted on the R platform (www.r-proje ct.org) (v3.2.0) and R packages. HPV positive infection rate, single-type HPV infec- tion rate and multi-type HPV infection rate were com- pared in three ways: stratifed by age group (< 30 years old, 30–40 years old, 40–50 years old, 50–60 years old, ≥ 60 Years) comparison, by every HPV subtype infection, and by long-term infection trend of all 21 HPV subtypes from 2014 to 2019. At the same time, the Fig. 1 TCT cytology test results’ distributions between positive positive rate of TCT infection in diferent age groups and negative HPV infection rates. The left group represents TCT was compared according to the same age stratifcation. distribution in HPV- positive infections, and the right group represents TCT distribution in HPV- negative infections. Dark blue Te secular trends for TCT and HPV positive infec- indicates the number of TCT-positive infections (including AGC, tion rates and their distribution in diferent age groups ASC, LSIL, HILM) in this group, and dark red indicates the number of were both analyzed during 2014–2019.
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