Vaginal and tumor microbiomes in gynecological cancer (Review)
- Authors:
- Mengzhen Han
- Na Wang
- Wenjie Han
- Meng Ban
- Tao Sun
- Junnan Xu
-
Affiliations: Department of Breast Medicine, Cancer Hospital of China Medical University, Liaoning Cancer Hospital, Shenyang, Liaoning 110000, P.R. China, Department of Breast Medicine, Cancer Hospital of China Medical University, Liaoning Cancer Hospital, Shenyang, Liaoning 110000, P.R. China, Liaoning Microhealth Biotechnology Co., Ltd., Shenyang, Liaoning 110000, P.R. China, Department of Breast Medicine, Cancer Hospital of Dalian University of Technology, Liaoning Cancer Hospital, Shenyang, Liaoning 110000, P.R. China, Department of Breast Medicine, Cancer Hospital of Dalian University of Technology, Liaoning Cancer Hospital, Shenyang, Liaoning 110000, P.R. China - Published online on: March 3, 2023 https://doi.org/10.3892/ol.2023.13739
- Article Number: 153
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Copyright: © Han et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Johnson JS, Spakowicz DJ, Hong BY, Petersen LM, Demkowicz P, Chen L, Leopold SR, Hanson BM, Agresta HO, Gerstein M, et al: Evaluation of 16S rRNA gene sequencing for species and strain-level microbiome analysis. Nat Commun. 10:50292019. View Article : Google Scholar : PubMed/NCBI | |
Rinninella E, Raoul P, Cintoni M, Franceschi F, Miggiano GAD, Gasbarrini A and Mele MC: What is the healthy gut microbiota composition? A changing ecosystem across age, environment, diet, and diseases. Microorganisms. 7:142019. View Article : Google Scholar : PubMed/NCBI | |
Einstein MH, Levine NF and Nevadunsky NS: Menopause and cancers. Endocrinol Metab Clin North Am. 44:603–617. 2015. View Article : Google Scholar : PubMed/NCBI | |
Wu Y, Sun W, Liu H and Zhang D: Age at menopause and risk of developing endometrial cancer: A meta-analysis. Biomed Res Int. 2019:85841302019.PubMed/NCBI | |
Liang Y, Chen M, Qin L, Wan B and Wang H: A meta-analysis of the relationship between vaginal microecology, human papillomavirus infection and cervical intraepithelial neoplasia. Infect Agent Cancer. 14:292019. View Article : Google Scholar : PubMed/NCBI | |
Gillet E, Meys JF, Verstraelen H, Verhelst R, De Sutter P, Temmerman M and Vanden Broeck D: Association between bacterial vaginosis and cervical intraepithelial neoplasia: Systematic review and meta-analysis. PLoS One. 7:e452012012. View Article : Google Scholar : PubMed/NCBI | |
Sepich-Poore GD, Zitvogel L, Straussman R, Hasty J, Wargo JA and Knight R: The microbiome and human cancer. Science. 371:eabc45522021. View Article : Google Scholar : PubMed/NCBI | |
Poore GD, Kopylova E, Zhu Q, Carpenter C, Fraraccio S, Wandro S, Kosciolek T, Janssen S, Metcalf J, Song SJ, et al: Microbiome analyses of blood and tissues suggest cancer diagnostic approach. Nature. 579:567–574. 2020. View Article : Google Scholar : PubMed/NCBI | |
Witkin SS, Linhares IM and Giraldo P: Bacterial flora of the female genital tract: function and immune regulation. Best Pract Res Clin Obstet Gynaecol. 21:347–354. 2007. View Article : Google Scholar : PubMed/NCBI | |
Lidbeck A and Nord CE: Lactobacilli and the normal human anaerobic microflora. Clin Infect Dis. 16 (Suppl 4):S181–S187. 1993. View Article : Google Scholar : PubMed/NCBI | |
Chee WJY, Chew SY and Than LTL: Vaginal microbiota and the potential of Lactobacillus derivatives in maintaining vaginal health. Microb Cell Fact. 19:2032020. View Article : Google Scholar : PubMed/NCBI | |
Wilson JD, Lee RA, Balen AH and Rutherford AJ: Bacterial vaginal flora in relation to changing oestrogen levels. Int J Std Aids. 18:308–311. 2007. View Article : Google Scholar : PubMed/NCBI | |
Barrientos-Duran A, Fuentes-Lopez A, de Salazar A, Plaza-Diaz J and Garcia F: Reviewing the composition of vaginal microbiota: Inclusion of nutrition and probiotic factors in the maintenance of eubiosis. Nutrients. 12:4192020. View Article : Google Scholar : PubMed/NCBI | |
Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, Karlebach S, Gorle R, Russell J, Tacket CO, et al: Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci USA. 108 Suppl 1 (Suppl 1):S4680–S4687. 2011. View Article : Google Scholar | |
Gajer P, Brotman RM, Bai G, Sakamoto J, Schutte UM, Zhong X, Koenig SS, Fu L, Ma ZS, Zhou X, et al: Temporal dynamics of the human vaginal microbiota. Sci Transl Med. 4:132ra522012. View Article : Google Scholar : PubMed/NCBI | |
De Gregorio PR, Parolin C, Abruzzo A, Luppi B, Protti M, Mercolini L, Silva JA, Giordani B, Marangoni A, Nader-Macías MEF and Vitali B: Biosurfactant from vaginal Lactobacillus crispatus BC1 as a promising agent to interfere with Candida adhesion. Microb Cell Fact. 19:1332020. View Article : Google Scholar : PubMed/NCBI | |
Jung H, Ehlers MM, Peters RPH, Lombaard H, Redelinghuys MJ, Bezuidenhoudt JE and Kock MM: Growth forms of Gardnerella spp. and Lactobacillus spp. On vaginal cells. Front Cell Infect Microbiol. 10:712020. View Article : Google Scholar : PubMed/NCBI | |
Aldunate M, Tyssen D, Johnson A, Zakir T, Sonza S, Moench T, Cone R and Tachedjian G: Vaginal concentrations of lactic acid potently inactivate HIV. J Antimicrob Chemother. 68:2015–2025. 2013. View Article : Google Scholar : PubMed/NCBI | |
Tamarelle J, Thiebaut ACM, de Barbeyrac B, Bebear C, Ravel J and Delarocque-Astagneau E: The vaginal microbiota and its association with human papillomavirus, Chlamydia trachomatis, Neisseria gonorrhoeae and Mycoplasma genitalium infections: A systematic review and meta-analysis. Clin Microbiol Infect. 25:35–47. 2019. View Article : Google Scholar : PubMed/NCBI | |
Witkin SS and Linhares IM: Why do lactobacilli dominate the human vaginal microbiota? BJOG. 124:606–611. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kyrgiou M, Mitra A and Moscicki AB: Does the vaginal microbiota play a role in the development of cervical cancer? Transl Res. 179:168–182. 2017. View Article : Google Scholar : PubMed/NCBI | |
Ilhan ZE, Laniewski P, Thomas N, Roe DJ, Chase DM and Herbst-Kralovetz MM: Deciphering the complex interplay between microbiota, HPV, inflammation and cancer through cervicovaginal metabolic profiling. EBioMedicine. 44:675–690. 2019. View Article : Google Scholar : PubMed/NCBI | |
Vornhagen J, Armistead B, Santana-Ufret V, Gendrin C, Merillat S, Coleman M, Quach P, Boldenow E, Alishetti V, Leonhard-Melief C, et al: Group B streptococcus exploits vaginal epithelial exfoliation for ascending infection. J Clin Invest. 128:1985–1999. 2018. View Article : Google Scholar : PubMed/NCBI | |
Scillato M, Spitale A, Mongelli G, Privitera GF, Mangano K, Cianci A, Stefani S and Santagati M: Antimicrobial properties of Lactobacillus cell-free supernatants against multidrug-resistant urogenital pathogens. Microbiologyopen. 10:e11732021. View Article : Google Scholar : PubMed/NCBI | |
Chen Y, Qiu X, Wang W, Li D, Wu A, Hong Z, Di W and Qiu L: Human papillomavirus infection and cervical intraepithelial neoplasia progression are associated with increased vaginal microbiome diversity in a Chinese cohort. BMC Infect Dis. 20:6292020. View Article : Google Scholar : PubMed/NCBI | |
Mitra A, MacIntyre DA, Marchesi JR, Lee YS, Bennett PR and Kyrgiou M: The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome. 4:582016. View Article : Google Scholar : PubMed/NCBI | |
Onderdonk AB, Delaney ML and Fichorova RN: The human microbiome during Bacterial Vaginosis. Clin Microbiol Rev. 29:223–238. 2016. View Article : Google Scholar : PubMed/NCBI | |
Mitchell C and Marrazzo J: Bacterial vaginosis and the cervicovaginal immune response. Am J Reprod Immunol. 71:555–563. 2014. View Article : Google Scholar : PubMed/NCBI | |
Doerflinger SY, Throop AL and Herbst-Kralovetz MM: Bacteria in the vaginal microbiome alter the innate immune response and barrier properties of the human vaginal epithelia in a species-specific manner. J Infect Dis. 209:1989–1999. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang Z, Xiao R, Huang J, Qin X, Hu D, Guo E, Liu C, Lu F, You L, Sun C and Chen G: The diversity of vaginal microbiota predicts neoadjuvant chemotherapy responsiveness in locally advanced cervical cancer. Microb Ecol. 84:302–313. 2022. View Article : Google Scholar : PubMed/NCBI | |
Klatt NR, Cheu R, Birse K, Zevin AS, Perner M, Noël-Romas L, Grobler A, Westmacott G, Xie IY, Butler J, et al: Vaginal bacteria modify HIV tenofovir microbicide efficacy in African women. Science. 356:938–945. 2017. View Article : Google Scholar : PubMed/NCBI | |
Wang KD, Xu DJ, Wang BY, Yan DH, Lv Z and Su JR: Inhibitory effect of vaginal Lactobacillus supernatants on cervical cancer cells. Probiotics Antimicrob Proteins. 10:236–242. 2018. View Article : Google Scholar : PubMed/NCBI | |
Motevaseli E, Shirzad M, Akrami SM, Mousavi AS, Mirsalehian A and Modarressi MH: Normal and tumour cervical cells respond differently to vaginal lactobacilli, independent of pH and lactate. J Med Microbiol. 62((Pt 7)): 1065–1072. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sungur T, Aslim B, Karaaslan C and Aktas B: Impact of Exopolysaccharides (EPSs) of Lactobacillus gasseri strains isolated from human vagina on cervical tumor cells (HeLa). Anaerobe. 47:137–144. 2017. View Article : Google Scholar : PubMed/NCBI | |
Palma E, Recine N, Domenici L, Giorgini M, Pierangeli A and Panici PB: Long-term Lactobacillus rhamnosus BMX 54 application to restore a balanced vaginal ecosystem: A promising solution against HPV-infection. BMC Infect Dis. 18:132018. View Article : Google Scholar : PubMed/NCBI | |
Gosmann C, Anahtar MN, Handley SA, Farcasanu M, Abu-Ali G, Bowman BA, Padavattan N, Desai C, Droit L, Moodley A, et al: Lactobacillus-Deficient cervicovaginal bacterial communities are associated with increased HIV Acquisition in Young South African Women. Immunity. 46:29–37. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kalia N, Singh J and Kaur M: Microbiota in vaginal health and pathogenesis of recurrent vulvovaginal infections: A critical review. Ann Clin Microbiol Antimicrob. 19:52020. View Article : Google Scholar : PubMed/NCBI | |
Borgogna JC, Shardell MD, Santori EK, Nelson TM, Rath JM, Glover ED, Ravel J, Gravitt PE, Yeoman CJ and Brotman RM: The vaginal metabolome and microbiota of cervical HPV-positive and HPV-negative women: A cross-sectional analysis. BJOG. 127:182–192. 2020. View Article : Google Scholar : PubMed/NCBI | |
Wei ZT, Chen HL, Wang CF, Yang GL, Han SM and Zhang SL: Depiction of vaginal microbiota in women with high-risk human papillomavirus infection. Front Public Health. 8:5872982021. View Article : Google Scholar : PubMed/NCBI | |
Uttley L, Whiteman BL, Woods HB, Harnan S, Philips ST and Cree IA; Early Cancer Detection Consortium, : Building the evidence base of blood-based biomarkers for early detection of cancer: A rapid systematic mapping review. EBioMedicine. 10:164–173. 2016. View Article : Google Scholar : PubMed/NCBI | |
Papageorgis P, Ozturk S, Lambert AW, Neophytou CM, Tzatsos A, Wong CK, Thiagalingam S and Constantinou AI: Targeting IL13Ralpha2 activates STAT6-TP63 pathway to suppress breast cancer lung metastasis. Breast Cancer Res. 17:982015. View Article : Google Scholar : PubMed/NCBI | |
Fang L, Lu W, Choi HH, Yeung SC, Tung JY, Hsiao CD, Fuentes-Mattei E, Menter D, Chen C, Wang L, et al: ERK2-Dependent phosphorylation of CSN6 is critical in colorectal cancer development. Cancer Cell. 28:183–197. 2015. View Article : Google Scholar : PubMed/NCBI | |
Laniewski P, Cui H, Roe DJ, Barnes D, Goulder A, Monk BJ, Greenspan DL, Chase DM and Herbst-Kralovetz MM: Features of the cervicovaginal microenvironment drive cancer biomarker signatures in patients across cervical carcinogenesis. Sci Rep. 9:73332019. View Article : Google Scholar : PubMed/NCBI | |
De Seta F, Campisciano G, Zanotta N, Ricci G and Comar M: The vaginal community state types microbiome-immune network as key factor for bacterial vaginosis and aerobic vaginitis. Front Microbiol. 10:24512019. View Article : Google Scholar : PubMed/NCBI | |
Recine N, Palma E, Domenici L, Giorgini M, Imperiale L, Sassu C, Musella A, Marchetti C, Muzii L and Benedetti Panici P: Restoring vaginal microbiota: Biological control of bacterial vaginosis. A prospective case-control study using Lactobacillus rhamnosus BMX 54 as adjuvant treatment against bacterial vaginosis. Arch Gynecol Obstet. 293:101–107. 2016. View Article : Google Scholar : PubMed/NCBI | |
De Alberti D, Russo R, Terruzzi F, Nobile V and Ouwehand AC: Lactobacilli vaginal colonisation after oral consumption of Respecta((R)) complex: A randomised controlled pilot study. Arch Gynecol Obstet. 292:861–867. 2015. View Article : Google Scholar : PubMed/NCBI | |
de Vrese M, Laue C, Papazova E, Petricevic L and Schrezenmeir J: Impact of oral administration of four Lactobacillus strains on Nugent score-systematic review and meta-analysis. Benef Microbes. 10:483–496. 2019. View Article : Google Scholar : PubMed/NCBI | |
Lev-Sagie A, Goldman-Wohl D, Cohen Y, Dori-Bachash M, Leshem A, Mor U, Strahilevitz J, Moses AE, Shapiro H, Yagel S and Elinav E: Vaginal microbiome transplantation in women with intractable bacterial vaginosis. Nat Med. 25:1500–1504. 2019. View Article : Google Scholar : PubMed/NCBI | |
Molijn A, Jenkins D, Chen W, Zhang X, Pirog E, Enqi W, Liu B, Schmidt J, Cui J, Qiao Y, et al: The complex relationship between human papillomavirus and cervical adenocarcinoma. Int J Cancer. 138:409–416. 2016. View Article : Google Scholar : PubMed/NCBI | |
Ho GY, Bierman R, Beardsley L, Chang CJ and Burk RD: Natural history of cervicovaginal papillomavirus infection in young women. N Engl J Med. 338:423–428. 1998. View Article : Google Scholar : PubMed/NCBI | |
Holly EA: Cervical intraepithelial neoplasia, cervical cancer, and HPV. Annu Rev Public Health. 17:69–84. 1996. View Article : Google Scholar : PubMed/NCBI | |
Norenhag J, Du J, Olovsson M, Verstraelen H, Engstrand L and Brusselaers N: The vaginal microbiota, human papillomavirus and cervical dysplasia: A systematic review and network meta-analysis. BJOG. 127:171–180. 2020. View Article : Google Scholar : PubMed/NCBI | |
Lee JE, Lee S, Lee H, Song YM, Lee K, Han MJ, Sung J and Ko G: Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS One. 8:e635142013. View Article : Google Scholar : PubMed/NCBI | |
Yang Q, Wang Y, Wei X, Zhu J, Wang X, Xie X and Lu W: The alterations of vaginal microbiome in HPV16 infection as identified by shotgun metagenomic sequencing. Front Cell Infect Microbiol. 10:2862020. View Article : Google Scholar : PubMed/NCBI | |
Zhang Z, Li T, Zhang D, Zong X, Bai H, Bi H and Liu Z: Distinction between vaginal and cervical microbiota in high-risk human papilloma virus-infected women in China. BMC Microbiol. 21:902021. View Article : Google Scholar : PubMed/NCBI | |
Egawa N and Doorbar J: The low-risk papillomaviruses. Virus Res. 231:119–127. 2017. View Article : Google Scholar : PubMed/NCBI | |
Vanska S, Luostarinen T, Lagheden C, Eklund C, Kleppe SN, Andrae B, Sparén P, Sundström K, Lehtinen M and Dillner J: Differing age-specific cervical cancer incidence between different types of human papillomavirus: Implications for predicting the impact of elimination programs. Am J Epidemiol. 190:506–514. 2021. View Article : Google Scholar : PubMed/NCBI | |
Huang X, Li C, Li F, Zhao J, Wan X and Wang K: Cervicovaginal microbiota composition correlates with the acquisition of high-risk human papillomavirus types. Int J Cancer. 143:621–634. 2018. View Article : Google Scholar : PubMed/NCBI | |
Brotman RM, Shardell MD, Gajer P, Tracy JK, Zenilman JM, Ravel J and Gravitt PE: Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J Infect Dis. 210:1723–1733. 2014. View Article : Google Scholar : PubMed/NCBI | |
Di Paola M, Sani C, Clemente AM, Iossa A, Perissi E, Castronovo G, Tanturli M, Rivero D, Cozzolino F, Cavalieri D, et al: Characterization of cervico-vaginal microbiota in women developing persistent high-risk Human Papillomavirus infection. Sci Rep. 7:102002017. View Article : Google Scholar : PubMed/NCBI | |
Mei L, Wang T, Chen Y, Wei D, Zhang Y, Cui T, Meng J, Zhang X, Liu Y, Ding L and Niu X: Dysbiosis of vaginal microbiota associated with persistent high-risk human papilloma virus infection. J Transl Med. 20:122022. View Article : Google Scholar : PubMed/NCBI | |
Lv P, Zhao F, Xu X, Xu J, Wang Q and Zhao Z: Correlation between common lower genital tract microbes and high-risk human papillomavirus infection. Can J Infect Dis Med Microbiol. 2019:96781042019. View Article : Google Scholar : PubMed/NCBI | |
Torcia MG: Interplay among vaginal microbiome, immune response and sexually transmitted viral infections. Int J Mol Sci. 20:2262019. View Article : Google Scholar | |
Mitra A, MacIntyre DA, Lee YS, Smith A, Marchesi JR, Lehne B, Bhatia R, Lyons D, Paraskevaidis E, Li JV, et al: Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci Rep. 5:168652015. View Article : Google Scholar : PubMed/NCBI | |
Mitra A, MacIntyre DA, Ntritsos G, Smith A, Tsilidis KK, Marchesi JR, Bennett PR, Moscicki AB and Kyrgiou M: The vaginal microbiota associates with the regression of untreated cervical intraepithelial neoplasia 2 lesions. Nat Commun. 11:19992020. View Article : Google Scholar : PubMed/NCBI | |
Tango CN, Seo SS, Kwon M, Lee DO, Chang HK and Kim MK: Taxonomic and functional differences in cervical microbiome associated with cervical cancer development. Sci Rep. 10:97202020. View Article : Google Scholar : PubMed/NCBI | |
Wu S, Ding X, Kong Y, Acharya S, Wu H, Huang C, Liang Y, Nong X and Chen H: The feature of cervical microbiota associated with the progression of cervical cancer among reproductive females. Gynecol Oncol. 163:348–357. 2021. View Article : Google Scholar : PubMed/NCBI | |
Łaniewski P, Barnes D, Goulder A, Cui H, Roe DJ, Chase DM and Herbst-Kralovetz MM: Linking cervicovaginal immune signatures, HPV and microbiota composition in cervical carcinogenesis in non-Hispanic and Hispanic women. Sci Rep. 8:75932018. View Article : Google Scholar : PubMed/NCBI | |
Mitra A, MacIntyre DA, Paraskevaidi M, Moscicki AB, Mahajan V, Smith A, Lee YS, Lyons D, Paraskevaidis E, Marchesi JR, et al: The vaginal microbiota and innate immunity after local excisional treatment for cervical intraepithelial neoplasia. Genome Med. 13:1762021. View Article : Google Scholar : PubMed/NCBI | |
Zhang H, Lu J, Lu Y, Cai Q, Liu H and Xu C: Cervical microbiome is altered in cervical intraepithelial neoplasia after loop electrosurgical excision procedure in China. Sci Rep. 8:49232018. View Article : Google Scholar : PubMed/NCBI | |
Parkin DM, Bray F, Ferlay J and Pisani P: Global Cancer Statistics, 2002. CA Cancer J Clin. 55:74–108. 2005. View Article : Google Scholar : PubMed/NCBI | |
Audirac-Chalifour A, Torres-Poveda K, Bahena-Roman M, Tellez-Sosa J, Martinez-Barnetche J, Cortina-Ceballos B, López-Estrada G, Delgado-Romero K, Burguete-García AI, Cantú D, et al: Cervical microbiome and cytokine profile at various stages of cervical cancer: A pilot study. PLoS One. 11:e01532742016. View Article : Google Scholar : PubMed/NCBI | |
Kang GU, Jung DR, Lee YH, Jeon SY, Han HS, Chong GO and Shin JH: Potential association between vaginal microbiota and cervical carcinogenesis in Korean Women: A cohort study. Microorganisms. 9:2942021. View Article : Google Scholar : PubMed/NCBI | |
Carlson KJ, Skates SJ and Singer DE: Screening for ovarian cancer. Ann Intern Med. 121:124–132. 1994. View Article : Google Scholar : PubMed/NCBI | |
Coburn SB, Bray F, Sherman ME and Trabert B: International patterns and trends in ovarian cancer incidence, overall and by histologic subtype. Int J Cancer. 140:2451–2460. 2017. View Article : Google Scholar : PubMed/NCBI | |
Nené NR, Reisel D, Leimbach A, Franchi D, Jones A, Evans I, Knapp S, Ryan A, Ghazali S, Timms JF, et al: Association between the cervicovaginal microbiome, BRCA1 mutation status, and risk of ovarian cancer: A case-control study. Lancet Oncol. 20:1171–1182. 2019. View Article : Google Scholar : PubMed/NCBI | |
Morikawa A, Kawabata A, Shirahige K, Akiyama T, Okamoto A and Sutani T: Altered cervicovaginal microbiota in premenopausal ovarian cancer patients. Gene. 811:1460832022. View Article : Google Scholar : PubMed/NCBI | |
Ely LK and Truong M: The role of opportunistic bilateral salpingectomy vs tubal occlusion or ligation for ovarian cancer prophylaxis. J Minim Invasive Gynecol. 24:371–378. 2017. View Article : Google Scholar : PubMed/NCBI | |
Cibula D, Widschwendter M, Majek O and Dusek L: Tubal ligation and the risk of ovarian cancer: Review and meta-analysis. Hum Reprod Update. 17:55–67. 2011. View Article : Google Scholar : PubMed/NCBI | |
Yoon SH, Kim SN, Shim SH, Kang SB and Lee SJ: Bilateral salpingectomy can reduce the risk of ovarian cancer in the general population: A meta-analysis. Eur J Cancer. 55:38–46. 2016. View Article : Google Scholar : PubMed/NCBI | |
Jacobson D, Moore K, Gunderson C, Rowland M, Austin R, Honap TP, Xu J and Warinner C: Shifts in gut and vaginal microbiomes are associated with cancer recurrence time in women with ovarian cancer. PeerJ. 9:e115742021. View Article : Google Scholar : PubMed/NCBI | |
Wong-Rolle A, Wei HK, Zhao C and Jin C: Unexpected guests in the tumor microenvironment: Microbiome in cancer. Protein Cell. 12:426–435. 2021. View Article : Google Scholar : PubMed/NCBI | |
Amant F, Moerman P, Neven P, Timmerman D, Van Limbergen E and Vergote I: Endometrial cancer. Lancet Oncol. 366:491–505. 2005. View Article : Google Scholar : PubMed/NCBI | |
Kim S, Seo H, Rahim MA, Lee S, Kim YS and Song HY: Changes in the microbiome of vaginal fluid after menopause in Korean Women. J Microbiol Biotechnol. 31:1490–1500. 2021. View Article : Google Scholar : PubMed/NCBI | |
Shardell M, Gravitt PE, Burke AE, Ravel J and Brotman RM: Association of vaginal microbiota with signs and symptoms of the genitourinary syndrome of menopause across reproductive stages. J Gerontol A Biol Sci Med Sci. 76:1542–1550. 2021. View Article : Google Scholar : PubMed/NCBI | |
Brotman RM, Shardell MD, Gajer P, Fadrosh D, Chang K, Silver MI, Viscidi RP, Burke AE, Ravel J and Gravitt PE: Association between the vaginal microbiota, menopause status, and signs of vulvovaginal atrophy. Menopause. 21:450–458. 2014. View Article : Google Scholar : PubMed/NCBI | |
Suarez SS and Pacey AA: Sperm transport in the female reproductive tract. Hum Reprod Update. 12:23–37. 2006. View Article : Google Scholar : PubMed/NCBI | |
Hansen LK, Becher N, Bastholm S, Glavind J, Ramsing M, Kim CJ, Romero R, Jensen JS and Uldbjerg N: The cervical mucus plug inhibits, but does not block, the passage of ascending bacteria from the vagina during pregnancy. Acta Obstet Gynecol Scand. 93:102–108. 2014. View Article : Google Scholar : PubMed/NCBI | |
Zervomanolakis I, Ott HW, Hadziomerovic D, Mattle V, Seeber BE, Virgolini I, Heute D, Kissler S, Leyendecker G and Wildt L: Physiology of upward transport in the human female genital tract. Ann N Y Acad Sci. 1101:1–20. 2007. View Article : Google Scholar : PubMed/NCBI | |
Garcia-Grau I, Simon C and Moreno I: Uterine microbiome-low biomass and high expectationsdagger. Biol Reprod. 101:1102–1114. 2019. View Article : Google Scholar : PubMed/NCBI | |
Mitchell CM, Haick A, Nkwopara E, Garcia R, Rendi M, Agnew K, Fredricks DN and Eschenbach D: Colonization of the upper genital tract by vaginal bacterial species in nonpregnant women. Am J Obstet Gynecol. 212:611e1–9. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chen C, Song X, Wei W, Zhong H, Dai J, Lan Z, Li F, Yu X, Feng Q, Wang Z, et al: The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 8:8752017. View Article : Google Scholar : PubMed/NCBI | |
Furukawa T, Jisaki F, Sakamuro D, Takegami T and Murayama T: Detection of human cytomegalovirus genome in uterus tissue. Arch Viro. 135:265–277. 1994. View Article : Google Scholar : PubMed/NCBI | |
Tobiasch E, Rabreau M, Geletneky K, Laruë-Charlus S, Severin F, Becker N and Schlehofer JR: Detection of adeno-associated virus DNA in human genital tissue and in material from spontaneous abortion. J Med Viro. 44:215–222. 1994. View Article : Google Scholar : PubMed/NCBI | |
Komaroff AL, Rizzo R and Ecker JL: Human Herpesviruses 6A and 6B in reproductive diseases. Front Immunol. 12:6489452021. View Article : Google Scholar : PubMed/NCBI | |
Callan T, Woodcock S and Huston WM: Ascension of Chlamydia is moderated by uterine peristalsis and the neutrophil response to infection. PLoS Comput Biol. 17:e10093652021. View Article : Google Scholar : PubMed/NCBI | |
Paavonen J, Aine R, Teisala K, Heinonen PK, Punnonen R, Lehtinen M, Miettinen A and Grönroos P: Chlamydial endometritis. J Clin Pathol. 38:726–732. 1985. View Article : Google Scholar : PubMed/NCBI | |
Moreno I, Cicinelli E, Garcia-Grau I, Gonzalez-Monfort M, Bau D, Vilella F, De Ziegler D, Resta L, Valbuena D and Simon C: The diagnosis of chronic endometritis in infertile asymptomatic women: A comparative study of histology, microbial cultures, hysteroscopy, and molecular microbiology. Am J Obstet Gynecol. 218:602e1–e16. 2018. View Article : Google Scholar : PubMed/NCBI | |
Smith JR, Wells C, Jolly M, Shah P, Savage M, Reginald P and Kitchen VS: Is endometrial infection with Candida albicans a cause of recurrent vaginal thrush? Genitourin Med. 69:295–296. 1993.PubMed/NCBI | |
Walther-António MR, Chen J, Multinu F, Hokenstad A, Distad TJ, Cheek EH, Keeney GL, Creedon DJ, Nelson H, Mariani A and Chia N: Potential contribution of the uterine microbiome in the development of endometrial cancer. Genome Med. 8:1222016. View Article : Google Scholar : PubMed/NCBI | |
Walsh DM, Hokenstad AN, Chen J, Sung J, Jenkins GD, Chia N, Nelson H, Mariani A and Walther-António MRS: Postmenopause as a key factor in the composition of the endometrial cancer microbiome (ECbiome). Sci Rep. 9:192132019. View Article : Google Scholar : PubMed/NCBI | |
Milde-Langosch K, Becker G and Löning T: Human papillomavirus and c-myc/c-erbB2 in uterine and vulvar lesions. Virchows Arch A Pathol Anat Histopathol. 419:479–485. 1991. View Article : Google Scholar : PubMed/NCBI | |
Yang HJ, Liu VW, Tsang PC, Yip AM, Ng TY, Cheung AN and Ngan HY: Comparison of human papillomavirus DNA levels in gynecological cancers: Implication for cancer development. Tumour Biol. 24:310–316. 2003. View Article : Google Scholar : PubMed/NCBI | |
Olesen TB, Svahn MF, Faber MT, Duun-Henriksen AK, Junge J, Norrild B and Kjaer SK: Prevalence of human papillomavirus in endometrial cancer: A systematic review and meta-analysis. Gynecol Oncol. 134:206–215. 2014. View Article : Google Scholar : PubMed/NCBI | |
Abu-Lubad MA, Jarajreh DA, Helaly GF, Alzoubi HM, Haddadin WJ, Dabobash MD, Albataineh EM, Aqel AA and Alnawaiseh NA: Human papillomavirus as an independent risk factor of invasive cervical and endometrial carcinomas in Jordan. J Infect Public Health. 13:613–618. 2020. View Article : Google Scholar : PubMed/NCBI | |
Jiang XF, Tang QL, Zou Y, Xu L, Zeng H, Chi C, Jiang JR and Zhang BZ: Does HBV infection increase risk of endometrial carcinoma? Asian Pac J Cancer Prev. 15:713–716. 2014. View Article : Google Scholar : PubMed/NCBI | |
Benharroch D, Klinkovich I, Piura B, Shaco-Levy R and Gopas J: Evidence of measles virus antigens and RNA in endometrial cancer. Eur J Obstet Gynecol Reprod Biol. 147:206–209. 2009. View Article : Google Scholar : PubMed/NCBI | |
Tsementzi D, Pena-Gonzalez A, Bai J, Hu YJ, Patel P, Shelton J, Dolan M, Arluck J, Khanna N, Conrad L, et al: Comparison of vaginal microbiota in gynecologic cancer patients pre- and post-radiation therapy and healthy women. Cancer Med. 9:3714–3724. 2020. View Article : Google Scholar : PubMed/NCBI | |
Nejman D, Livyatan I, Fuks G, Gavert N, Zwang Y, Geller LT, Rotter-Maskowitz A, Weiser R, Mallel G, Gigi E, et al: The human tumor microbiome is composed of tumor type-specific intracellular bacteria. Science. 368:973–980. 2020. View Article : Google Scholar : PubMed/NCBI | |
Tzeng A, Sangwan N, Jia M, Liu CC, Keslar KS, Downs-Kelly E, Fairchild RL, Al-Hilli Z, Grobmyer SR and Eng C: Human breast microbiome correlates with prognostic features and immunological signatures in breast cancer. Genome Med. 13:602021. View Article : Google Scholar : PubMed/NCBI | |
Ma J, Gnanasekar A, Lee A, Li WT, Haas M, Wang-Rodriguez J, Chang EY, Rajasekaran M and Ongkeko WM: Influence of intratumor microbiome on clinical outcome and immune processes in prostate cancer. Cancers (Basel). 12:25242020. View Article : Google Scholar : PubMed/NCBI | |
Pushalkar S, Hundeyin M, Daley D, Zambirinis CP, Kurz E, Mishra A, Mohan N, Aykut B, Usyk M, Torres LE, et al: The pancreatic cancer microbiome promotes oncogenesis by induction of innate and adaptive immune suppression. Cancer Discov. 8:403–416. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gnanasekar A, Castaneda G, Iyangar A, Magesh S, Perez D, Chakladar J, Li WT, Bouvet M, Chang EY and Ongkeko WM: The intratumor microbiome predicts prognosis across gender and subtypes in papillary thyroid carcinoma. Comput Struct Biotechnol J. 19:1986–1997. 2021. View Article : Google Scholar : PubMed/NCBI | |
Kostic AD, Gevers D, Pedamallu CS, Michaud M, Duke F, Earl AM, Ojesina AI, Jung J, Bass AJ, Tabernero J, et al: Genomic analysis identifies association of Fusobacterium with colorectal carcinoma. Genome Res. 22:292–298. 2012. View Article : Google Scholar : PubMed/NCBI | |
Del Castillo E, Meier R, Chung M, Koestler DC, Chen T, Paster BJ, Charpentier KP, Kelsey KT, Izard J and Michaud DS: The microbiomes of pancreatic and duodenum tissue overlap and are highly subject specific but differ between pancreatic cancer and noncancer subjects. Cancer Epidemiol Biomarkers Prev. 28:370–383. 2019. View Article : Google Scholar : PubMed/NCBI | |
Banerjee S, Tian T, Wei Z, Shih N, Feldman MD, Alwine JC, Coukos G and Robertson ES: The ovarian cancer oncobiome. Oncotarget. 8:36225–36245. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang PP, Zhou L, Cao JS, Li YP, Zeng Z, Sun N, Shen L, Zhu HY, Ruan Y, Zha WT, et al: Possible epithelial ovarian cancer association with HPV18 or HPV33 Infection. Asian Pac J Cancer Prev. 17:2959–2964. 2016.PubMed/NCBI | |
Hassan ZK, Hafez MM, Kamel MM and Zekri AR: Human papillomavirus genotypes and methylation of CADM1, PAX1, MAL and ADCYAP1 genes in epithelial ovarian cancer patients. Asian Pac J Cancer Prev. 18:169–176. 2017.PubMed/NCBI | |
Shanmughapriya S, Senthilkumar G, Vinodhini K, Das BC, Vasanthi N and Natarajaseenivasan K: Viral and bacterial aetiologies of epithelial ovarian cancer. Eur J Clin Microbiol Infect Dis. 31:2311–2317. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jonsson S, Oda H, Lundin E, Olsson J and Idahl A: Chlamydia trachomatis, Chlamydial heat shock protein 60 and anti-chlamydial antibodies in women with epithelial ovarian tumors. Transl Oncol. 11:546–551. 2018. View Article : Google Scholar : PubMed/NCBI | |
Idahl A, Lundin E, Elgh F, Jurstrand M, Moller JK, Marklund I, Lindgren P and Ottander U: Chlamydia trachomatis, Mycoplasma genitalium, Neisseria gonorrhoeae, human papillomavirus, and polyomavirus are not detectable in human tissue with epithelial ovarian cancer, borderline tumor, or benign conditions. Am J Obstet Gynecol. 202:71e1–6. 2010. View Article : Google Scholar : PubMed/NCBI | |
Zhou B, Sun C, Huang J, Xia M, Guo E, Li N, Lu H, Shan W, Wu Y, Li Y, et al: The biodiversity composition of microbiome in ovarian carcinoma patients. Sci Rep. 9:16912019. View Article : Google Scholar : PubMed/NCBI | |
Wang Q, Zhao L, Han L, Fu G, Tuo X, Ma S, Li Q, Wang Y, Liang D, Tang M, et al: The differential distribution of bacteria between cancerous and noncancerous ovarian tissues in situ. J Ovarian Res. 13:82020. View Article : Google Scholar : PubMed/NCBI | |
Brewster WR, Burkett WC, Ko EM, Bae-Jump V, Nicole McCoy A and Keku TO: An evaluation of the microbiota of the upper reproductive tract of women with and without epithelial ovarian cancer. Gynecol Oncol Rep. 42:1010172022. View Article : Google Scholar : PubMed/NCBI | |
Moreno I, Codoñer FM, Vilella F, Valbuena D, Martinez-Blanch JF, Jimenez-Almazán J, Alonso R, Alamá P, Remohí J, Pellicer A, et al: Evidence that the endometrial microbiota has an effect on implantation success or failure. Am J Obstet Gynecol. 216:684–703. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kyono K, Hashimoto T, Nagai Y and Sakuraba Y: Analysis of endometrial microbiota by 16S ribosomal RNA gene sequencing among infertile patients: a single-center pilot study. Reprod Med Biol. 17:297–306. 2018. View Article : Google Scholar : PubMed/NCBI | |
Wang L, Yang J, Su H, Shi L, Chen B and Zhang S: Endometrial microbiota from endometrial cancer and paired pericancer tissues in postmenopausal women: Differences and clinical relevance. Menopause. 29:1168–1175. 2022. View Article : Google Scholar : PubMed/NCBI | |
Lu W, He F, Lin Z, Liu S, Tang L, Huang Y and Hu Z: Dysbiosis of the endometrial microbiota and its association with inflammatory cytokines in endometrial cancer. Int J Cancer. 148:1708–1716. 2021. View Article : Google Scholar : PubMed/NCBI | |
Caselli E, Soffritti I, D'Accolti M, Piva I, Greco P and Bonaccorsi G: Atopobium vaginae and porphyromonas somerae induce proinflammatory cytokines expression in endometrial cells: A possible implication for endometrial cancer? Cancer Manag Res. 11:8571–8575. 2019. View Article : Google Scholar : PubMed/NCBI | |
Deligdisch L, Marin T, Lee AT, Etkind P, Holland JF, Melana S and Pogo BG: Human mammary tumor virus (HMTV) in endometrial carcinoma. Int J Gynecol Cancer. 23:1423–1428. 2013. View Article : Google Scholar : PubMed/NCBI | |
Li C, Gu Y, He Q, Huang J, Song Y, Wan X and Li Y: Integrated analysis of microbiome and transcriptome data reveals the interplay between commensal bacteria and fibrin degradation in endometrial cancer. Front Cell Infect Microbiol. 11:7485582021. View Article : Google Scholar : PubMed/NCBI |