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Evaluation of the Associations Between Cervical Microbiota and HPV Infection, Clearance, and Persistence in Cytologically Normal

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Evaluation of the Associations Between Cervical Microbiota and HPV Infection, Clearance, and Persistence in Cytologically Normal Published OnlineFirst November 21, 2018; DOI: 10.1158/1940-6207.CAPR-18-0233 Research Article Cancer Prevention Research Evaluation of the Associations Between Cervical Microbiota and HPV Infection, Clearance, and Persistence in Cytologically Normal Women Wu Ritu1, Wu Enqi1, Siriguleng Zheng2, Jiandong Wang3, Yaqin Ling1, and Yan Wang3 Abstract The aim of this study was to investigate the associa- Pseudomonas aeruginosa were associated with baseline tions between cervical microbiota and different human HPV negativity. For HPV-positive women, the base- papillomavirus (HPV) infection statuses in cytological- line abundance of Actinomyces was negatively associ- ly normal women. The cervical microbiota of HPV- ated with new HPV infection, Alloprevotella tannerae, positive or -negative women with a normal cytologic Prevotella nigrescens,andPrevotella oulorum;and diagnosis was characterized and compared using 16S Dialister invisus were positively associated with new rDNA-based high-throughput sequencing, and the HPV-type infection within the year of follow-up. differences in cervical microbiota associated with new Lactobacillus delbrueckii was found to be negatively acquisition, persistence, and clearances of HPV geno- associated with persistent HPV infection and 9 taxa types were analyzed via one-year follow-up. The results belonging to Prevotella, Dialister,andLachnospiraceae showed that the cervical microbial richness of HPV- were found to be positively associated with persis- positive women was lower than for HPV-negative tence, and/or negatively associated with clearance of women, and the difference was more significant in the HPV types. We also observed 10 novel taxa associated postmenopausal group relative to the premenopausal with the clearance/persistence of HPV that had not group. Ureaplasma parvum and related taxa were been reported elsewhere. Those taxa associated with associated with baseline HPV positivity, while different infection statuses of HPV could be used as a Brochothrix, Diplorickettsia, Ezakiella, Faecalibacterium, biomarker to help predict the risk of developing and Fusobacterium genera and their related taxa and persistent HPV infection. Introduction malignancies (1). It is known that HPV infection is very common in sexually active women, and the infecting HPVs Cervical cancer is one of the most common cancers can usually be spontaneously eliminated from individuals among women worldwide, and persistent infection within 6 to 18 months. Only a small proportion of infected with high-risk human papillomavirus (HPV) types has women retain the virus, and this could lead to the devel- been confirmed to be the necessary factor for developing opment of cervical intraepithelial neoplasia (CIN) and cervical carcinoma (2). The mechanism by which some 1Key Laboratory of Ethnomedicine (Minzu University of China), Ministry of individuals develop a persistent HPV infection that goes on Education, Beijing, China. 2Department of Information Technology, Polytechnic to develop into clinically significant disease, however, College, Beijing, China. 3Department of Gynecological Oncology, Beijing Obstet- remains largely unclear. rics and Gynecology Hospital of Capital Medical University, Beijing, China. Emerging evidence shows that the human microbiome Note: Supplementary data for this article are available at Cancer Prevention can mirror the host's physiology and that it plays an Research Online (http://cancerprevres.aacrjournals.org/). important role in human health (3). Several cross-sectional W. Ritu and W. Enqi contributed equally to this article. studies addressing the association between the microbiota Corresponding Authors: Yan Wang, Beijing Obstetrics and Gynecology Hospital in the female reproductive tract and HPV infection and of Capital Medical University, Beijing 100006, China. Phone: 186-1065-3059; Fax: 010-6512-1602; E-mail: [email protected]; and Yaqin Ling, Key Laboratory related diseases have been undertaken, and they clearly of Ethnomedicine (Minzu University of China), Ministry of Education, Beijing show that there are significant differences between HPV- 100081, P. R. China. Phone: 188-1022-2674; E-mail: [email protected] negative and -positive women and between healthy wom- doi: 10.1158/1940-6207.CAPR-18-0233 en and women with HPV-related diseases with respect Ó2018 American Association for Cancer Research. to microbial structure, diversity, and species composition www.aacrjournals.org OF1 Downloaded from cancerpreventionresearch.aacrjournals.org on October 1, 2021. © 2018 American Association for Cancer Research. Published OnlineFirst November 21, 2018; DOI: 10.1158/1940-6207.CAPR-18-0233 Ritu et al. (4–6). Regarding the comparison between HPV-positive in the Beijing Obstetrics and Gynecology Hospital (Beijing, and -negative women, the studies in a community of China), from August to September 2016. Written and Korean and Chinese women both found HPV-positive verbal consent were obtained from each participant. The women had significantly higher microbial diversity than exclusive criteria included current pregnancy, sexual inter- HPV-negative women (4, 5). Lee and colleagues also course or washout within 3 days, oral or vaginal usage of observed the HPV-positive women have significantly less antibiotics within 2 weeks, previous history of cervical or Lactobacillus spp. than their counterparts, and identified other lower genital cancer, previous hysterectomy, or Sneathia spp. to be a microbiological marker of HPV destructive therapy of the cervix. To eliminate the impact infection (4). In the comparison between healthy women of the potential change in microbiota that is driven by and women with HPV-related diseases, the studies of Oh cervical lesions, only women with normal cytologic results and colleagues (6) and Audirac-Chalifour and collea- were included in this study. All of the participating women gues (7) conclude that women with CIN had a higher were asked to attend the 1-year follow-up visit for repeated vaginal diversity than healthy controls. The presence of HPV testing. Anaerococcus vaginae, Garderella vaginalis, and L. iners in the Risk factor information of lifestyle profile (such as age, absence of L. crispatus were identified to be the most high- cigarette smoking, parity, menstrual status, and use of risk combination for development of CIN. In addition, hormonal/oral contraceptives) was collected with a ques- Brotman and coworkers performed a longitudinal tionnaire while waiting for the physical examination. study in a North American cohort of 32 sexually active, Three cervical swab specimens were collected from premenopausal women over the course of 16 weeks using each participant by cyto-brush (Qiagen) during routine a twice-weekly interval of evaluation to describe the pelvic examination. The first specimens were used for temporal relationship between vaginal microbiota and cytologic diagnosis (SurePath Liquid System, BD Diag- HPV detection. Using hierarchical taxonomic clustering, nostics TriPath); the second specimens were stored in the vaginal microbial profile of each woman was classified standard transport medium (STM) for HPV testing; and into a total of five community state types (CST). The the third specimens were stored in 4 mol/L guanidine authors found that the CST was associated with changes thiocyanate solution for further microbiota analysis. The in HPV status and a low lactobacillus community with high specimens for microbiota analysis were frozen at À20C proportions of the genera Atopobium was found to have the immediately, and then transferred to the laboratory slowest rate of HPV clearance (8). within 24 hours and stored at À80CbeforeDNA The aforementioned evidence indicates that the cervi- extraction. covaginal microbiota plays a substantial role in the infec- DNA was extracted from the residual STM-stored cervical tion and clearance of HPV virus in the reproductive tract specimens using the QiAmp Mini DNA Kit (Qiagen) in and constitutes a new biomarker reservoir to predict the accordance with the manufacturer's recommendations. persistence or regression of HPV. So far, however, only a Total bacterial DNA was extracted from samples using few longitudinal studies concerning associations between the Power Soil DNA Isolation Kit (MO BIO Laboratories) cervicovaginal microbiota and HPV infection/clearance according to the manufacturer's protocol. DNA quality and have been conducted, and they were of very limited sample quantity were assessed using the ratios of 260 nm/280 nm size (9, 10). and 260 nm/230 nm. The DNA was then stored at À80C To investigate the correlation between cervicovaginal until further processing. microbiota and HPV infection status, particularly in asymptomatic women, we herein characterized and com- HPV assay and genotyping pared the composition of the cervical microbiota of 144 Cervical swab specimens stored in STM were tested by HPV-positive or -negative women with a normal cytologic Hybrid Capture 2 (HC2;Qiagen), using both the high- diagnosis, using 16S rDNA-based high-throughput risk (HR) panel of 13 pooled types (HPV16, 18, 31, 33, sequencing; and the differences in cervical microbiota 35, 39, 45, 51, 52, 56, 58, 59, and 68) and the low-risk associated with new acquisition, persistence, and clear- (LR) panel (types 6, 11, 42, 43, and 44). Samples were ances of HPV were analyzed throughout one year of processed according to the manufacturer's instructions follow-up. and considered positive if they reached the threshold value of at least 1.0 pg/mL of HPV
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