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Published in: Virology Journal 1/2023

Open Access 01-12-2023 | Human Papillomavirus | Review

The interplay between human papillomavirus and vaginal microbiota in cervical cancer development

Authors: Kimia Sharifian, Zabihollah Shoja, Somayeh Jalilvand

Published in: Virology Journal | Issue 1/2023

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Abstract

Over the past few decades, we have grown accustomed to the idea that human papillomavirus can cause tumors. The genetic and environmental factors that make the difference between elimination of viral infection and the development of cancer are therefore an area of active investigation at present. Microbiota has emerged as an important factor that may affect this balance by increasing or decreasing the ability of viral infection to promote. The female reproductive system has its specific microbiota that helps to maintain health and prevent infection with pathogens. In contrast to other mucosal sites, the vaginal microbiota typically has low diversity and contains few Lactobacillus spp. which by using high-throughput 16s rRNA gene sequencing, classified into five different community state types. According to emerging information, increased diversity of vaginal microbiota and reduced abundance of Lactobacillus spp. contribute to HPV acquisition, persistence, and development of cervical cancer. In this review, the role of normal female reproductive tract microbiota in health, mechanisms which dysbiosis can cause diseases through interaction with microbes and several therapeutic approaches were addressed.
Literature
1.
go back to reference International Agency for Research on Cancer. GLOBOCAN. Estimated cancer incidence. Mor Prevalence Worldwide in. 2020;2020(2020):2012. International Agency for Research on Cancer. GLOBOCAN. Estimated cancer incidence. Mor Prevalence Worldwide in. 2020;2020(2020):2012.
2.
go back to reference Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49.PubMedCrossRef Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49.PubMedCrossRef
3.
go back to reference Schiller JT, Lowy DR. Virus infection and human cancer: an overview. Recent Results Cancer Res Fortschritte der Krebsforschung Progres dans les recherches sur le cancer. 2014;193:1–10.PubMed Schiller JT, Lowy DR. Virus infection and human cancer: an overview. Recent Results Cancer Res Fortschritte der Krebsforschung Progres dans les recherches sur le cancer. 2014;193:1–10.PubMed
4.
go back to reference Schiller JT, Lowy DR. An Introduction to Virus Infections and Human Cancer. Recent Results Cancer Res Fortschritte der Krebsforschung Progres dans les recherches sur le cancer. 2021;217:1–11.PubMed Schiller JT, Lowy DR. An Introduction to Virus Infections and Human Cancer. Recent Results Cancer Res Fortschritte der Krebsforschung Progres dans les recherches sur le cancer. 2021;217:1–11.PubMed
5.
go back to reference Vyshenska D, Lam KC, Shulzhenko N, Morgun A, editors. Interplay between viruses and bacterial microbiota in cancer development. Seminars in immunology; 2017: Elsevier. Vyshenska D, Lam KC, Shulzhenko N, Morgun A, editors. Interplay between viruses and bacterial microbiota in cancer development. Seminars in immunology; 2017: Elsevier.
6.
go back to reference Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A, Wheadon M, et al. Commensal microbes and interferon-λ determine persistence of enteric murine norovirus infection. Science. 2015;347(6219):266–9.PubMedCrossRef Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A, Wheadon M, et al. Commensal microbes and interferon-λ determine persistence of enteric murine norovirus infection. Science. 2015;347(6219):266–9.PubMedCrossRef
7.
8.
go back to reference Konrad H, Rattenborg C. Combined action of laryngeal muscles. Acta Otolaryngol. 1969;67(2–6):646–9.PubMedCrossRef Konrad H, Rattenborg C. Combined action of laryngeal muscles. Acta Otolaryngol. 1969;67(2–6):646–9.PubMedCrossRef
9.
go back to reference Situnayake R, Thurnham D, Kootathep S, Chirico S, Lunec J, Davis M, et al. Chain breaking antioxidant status in rheumatoid arthritis: clinical and laboratory correlates. Ann Rheum Dis. 1991;50(2):81–6.PubMedPubMedCentralCrossRef Situnayake R, Thurnham D, Kootathep S, Chirico S, Lunec J, Davis M, et al. Chain breaking antioxidant status in rheumatoid arthritis: clinical and laboratory correlates. Ann Rheum Dis. 1991;50(2):81–6.PubMedPubMedCentralCrossRef
10.
go back to reference Ogunrinola GA, Oyewale JO, Oshamika OO, Olasehinde GI. The human microbiome and its impacts on health. Int J Microbiol. 2020;2020. Ogunrinola GA, Oyewale JO, Oshamika OO, Olasehinde GI. The human microbiome and its impacts on health. Int J Microbiol. 2020;2020.
11.
go back to reference Aviles-Jimenez F, Yu G, Torres-Poveda K, Madrid-Marina V, Torres J. On the search to elucidate the role of microbiota in the genesis of cancer: the cases of gastrointestinal and cervical cancer. Arch Med Res. 2017;48(8):754–65.PubMedCrossRef Aviles-Jimenez F, Yu G, Torres-Poveda K, Madrid-Marina V, Torres J. On the search to elucidate the role of microbiota in the genesis of cancer: the cases of gastrointestinal and cervical cancer. Arch Med Res. 2017;48(8):754–65.PubMedCrossRef
13.
go back to reference Busnelli M, Manzini S, Chiesa G. The gut microbiota affects host pathophysiology as an endocrine organ: a focus on cardiovascular disease. Nutrients. 2020;12(1):79.CrossRef Busnelli M, Manzini S, Chiesa G. The gut microbiota affects host pathophysiology as an endocrine organ: a focus on cardiovascular disease. Nutrients. 2020;12(1):79.CrossRef
14.
go back to reference Brianti P, De Flammineis E, Mercuri SR. Review of HPV-related diseases and cancers. New Microbiol. 2017;40(2):80–5.PubMed Brianti P, De Flammineis E, Mercuri SR. Review of HPV-related diseases and cancers. New Microbiol. 2017;40(2):80–5.PubMed
16.
go back to reference Van Doorslaer K, Chen Z, Bernard H-U, Chan PK, DeSalle R, Dillner J, et al. ICTV virus taxonomy profile: Papillomaviridae. J Gen Virol. 2018;99(8):989–90.PubMedPubMedCentralCrossRef Van Doorslaer K, Chen Z, Bernard H-U, Chan PK, DeSalle R, Dillner J, et al. ICTV virus taxonomy profile: Papillomaviridae. J Gen Virol. 2018;99(8):989–90.PubMedPubMedCentralCrossRef
17.
go back to reference De Villiers E-M, Fauquet C, Broker TR, Bernard H-U, Zur HH. Classification of papillomaviruses. Virology. 2004;324(1):17–27.PubMedCrossRef De Villiers E-M, Fauquet C, Broker TR, Bernard H-U, Zur HH. Classification of papillomaviruses. Virology. 2004;324(1):17–27.PubMedCrossRef
19.
20.
go back to reference Happel A-U, Varsani A, Balle C, Passmore J-A, Jaspan H. The vaginal virome—balancing female genital tract bacteriome, mucosal immunity, and sexual and reproductive health outcomes? Viruses. 2020;12(8):832.PubMedPubMedCentralCrossRef Happel A-U, Varsani A, Balle C, Passmore J-A, Jaspan H. The vaginal virome—balancing female genital tract bacteriome, mucosal immunity, and sexual and reproductive health outcomes? Viruses. 2020;12(8):832.PubMedPubMedCentralCrossRef
21.
go back to reference Molina-Pineda A, López-Cardona MG, Limón-Toledo LP, Cantón-Romero JC, Martínez-Silva MG, Ramos-Sánchez HV, et al. High frequency of HPV genotypes 59, 66, 52, 51, 39 and 56 in women from Western Mexico. BMC Infect Dis. 2020;20(1):1–10.CrossRef Molina-Pineda A, López-Cardona MG, Limón-Toledo LP, Cantón-Romero JC, Martínez-Silva MG, Ramos-Sánchez HV, et al. High frequency of HPV genotypes 59, 66, 52, 51, 39 and 56 in women from Western Mexico. BMC Infect Dis. 2020;20(1):1–10.CrossRef
22.
go back to reference Shiels MS, Kreimer AR, Coghill AE, Darragh TM, Devesa SS. Anal cancer incidence in the United States, 1977–2011: distinct patterns by histology and behavior. Cancer Epidemiol Prevent Biomark. 2015;24(10):1548–56.CrossRef Shiels MS, Kreimer AR, Coghill AE, Darragh TM, Devesa SS. Anal cancer incidence in the United States, 1977–2011: distinct patterns by histology and behavior. Cancer Epidemiol Prevent Biomark. 2015;24(10):1548–56.CrossRef
23.
go back to reference Control CfD, Prevention. Cancers associated with human papillomavirus. United States—2011–2015 USCS data brief. 2018(4). Control CfD, Prevention. Cancers associated with human papillomavirus. United States—2011–2015 USCS data brief. 2018(4).
24.
go back to reference de Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in 2018: a worldwide incidence analysis. Lancet Glob Health. 2020;8(2):e180–90.PubMedCrossRef de Martel C, Georges D, Bray F, Ferlay J, Clifford GM. Global burden of cancer attributable to infections in 2018: a worldwide incidence analysis. Lancet Glob Health. 2020;8(2):e180–90.PubMedCrossRef
25.
go back to reference Bosch FX, De Sanjosé S. Chapter 1: Human papillomavirus and cervical cancer—burden and assessment of causality. JNCI Monogr. 2003;2003(31):3–13. Bosch FX, De Sanjosé S. Chapter 1: Human papillomavirus and cervical cancer—burden and assessment of causality. JNCI Monogr. 2003;2003(31):3–13.
26.
go back to reference Castanheira CP, Sallas ML, Nunes RAL, Lorenzi NPC, Termini L. Microbiome and cervical cancer. Pathobiology. 2021:1–11. Castanheira CP, Sallas ML, Nunes RAL, Lorenzi NPC, Termini L. Microbiome and cervical cancer. Pathobiology. 2021:1–11.
27.
28.
go back to reference Anderson C, Lee A, McLaren K, Cairns S, Cowen C, McQueen F, et al. Level of agreement and biopsy correlation using two-and three-tier systems to grade cervical dyskaryosis. Cytopathology. 2004;15(5):256–62.PubMedCrossRef Anderson C, Lee A, McLaren K, Cairns S, Cowen C, McQueen F, et al. Level of agreement and biopsy correlation using two-and three-tier systems to grade cervical dyskaryosis. Cytopathology. 2004;15(5):256–62.PubMedCrossRef
29.
go back to reference Ostör A. Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol. 1993;12(2):186–92.PubMedCrossRef Ostör A. Natural history of cervical intraepithelial neoplasia: a critical review. Int J Gynecol Pathol. 1993;12(2):186–92.PubMedCrossRef
30.
go back to reference Kyrgiou M, Mitra A, Moscicki A-B. Does the vaginal microbiota play a role in the development of cervical cancer? Transl Res. 2017;179:168–82.PubMedCrossRef Kyrgiou M, Mitra A, Moscicki A-B. Does the vaginal microbiota play a role in the development of cervical cancer? Transl Res. 2017;179:168–82.PubMedCrossRef
31.
go back to reference Sasagawa T, Takagi H, Makinoda S. Immune responses against human papillomavirus (HPV) infection and evasion of host defense in cervical cancer. J Infect Chemother. 2012;18(6):807–15.PubMedCrossRef Sasagawa T, Takagi H, Makinoda S. Immune responses against human papillomavirus (HPV) infection and evasion of host defense in cervical cancer. J Infect Chemother. 2012;18(6):807–15.PubMedCrossRef
32.
go back to reference Boda D, Docea AO, Calina D, Ilie MA, Caruntu C, Zurac S, et al. Human papilloma virus: apprehending the link with carcinogenesis and unveiling new research avenues. Int J Oncol. 2018;52(3):637–55.PubMedPubMedCentral Boda D, Docea AO, Calina D, Ilie MA, Caruntu C, Zurac S, et al. Human papilloma virus: apprehending the link with carcinogenesis and unveiling new research avenues. Int J Oncol. 2018;52(3):637–55.PubMedPubMedCentral
33.
go back to reference Lin L, Benard VB, Greek A, Hawkins NA, Roland KB, Saraiya M. Racial and ethnic differences in human papillomavirus positivity and risk factors among low-income women in Federally Qualified Health Centers in the United States. Prev Med. 2015;81:258–61.PubMedPubMedCentralCrossRef Lin L, Benard VB, Greek A, Hawkins NA, Roland KB, Saraiya M. Racial and ethnic differences in human papillomavirus positivity and risk factors among low-income women in Federally Qualified Health Centers in the United States. Prev Med. 2015;81:258–61.PubMedPubMedCentralCrossRef
34.
go back to reference Chen C, Song X, Wei W, Zhong H, Dai J, Lan Z, et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 2017;8(1):1–11. Chen C, Song X, Wei W, Zhong H, Dai J, Lan Z, et al. The microbiota continuum along the female reproductive tract and its relation to uterine-related diseases. Nat Commun. 2017;8(1):1–11.
35.
go back to reference Łaniewski P, Ilhan ZE, Herbst-Kralovetz MM. The microbiome and gynaecological cancer development, prevention and therapy. Nat Rev Urol. 2020;17(4):232–50.PubMedPubMedCentralCrossRef Łaniewski P, Ilhan ZE, Herbst-Kralovetz MM. The microbiome and gynaecological cancer development, prevention and therapy. Nat Rev Urol. 2020;17(4):232–50.PubMedPubMedCentralCrossRef
36.
go back to reference Mitra A, MacIntyre DA, Marchesi JR, Lee YS, Bennett PR, Kyrgiou M. The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome. 2016;4(1):1–15.CrossRef Mitra A, MacIntyre DA, Marchesi JR, Lee YS, Bennett PR, Kyrgiou M. The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome. 2016;4(1):1–15.CrossRef
37.
go back to reference Younes JA, Lievens E, Hummelen R, van der Westen R, Reid G, Petrova MI. Women and their microbes: the unexpected friendship. Trends Microbiol. 2018;26(1):16–32.PubMedCrossRef Younes JA, Lievens E, Hummelen R, van der Westen R, Reid G, Petrova MI. Women and their microbes: the unexpected friendship. Trends Microbiol. 2018;26(1):16–32.PubMedCrossRef
39.
go back to reference Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proc Natil Acad Sci USA. 2011;108(Suppl 1):4680–7.CrossRef Ravel J, Gajer P, Abdo Z, Schneider GM, Koenig SS, McCulle SL, et al. Vaginal microbiome of reproductive-age women. Proc Natil Acad Sci USA. 2011;108(Suppl 1):4680–7.CrossRef
40.
go back to reference Hickey RJ, Zhou X, Pierson JD, Ravel J, Forney LJ. Understanding vaginal microbiome complexity from an ecological perspective. Transl Res. 2012;160(4):267–82.PubMedPubMedCentralCrossRef Hickey RJ, Zhou X, Pierson JD, Ravel J, Forney LJ. Understanding vaginal microbiome complexity from an ecological perspective. Transl Res. 2012;160(4):267–82.PubMedPubMedCentralCrossRef
41.
go back to reference Łaniewski P, Herbst-Kralovetz M. Vagina. Encyclopedia of Reproduction. Amsterdam: Elsevier; 2018. p. 353–9.CrossRef Łaniewski P, Herbst-Kralovetz M. Vagina. Encyclopedia of Reproduction. Amsterdam: Elsevier; 2018. p. 353–9.CrossRef
42.
go back to reference Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Nikita L, et al. The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome. 2014;2(1):1–19. Romero R, Hassan SS, Gajer P, Tarca AL, Fadrosh DW, Nikita L, et al. The composition and stability of the vaginal microbiota of normal pregnant women is different from that of non-pregnant women. Microbiome. 2014;2(1):1–19.
43.
go back to reference Brotman RM, Shardell MD, Gajer P, Tracy JK, Zenilman JM, Ravel J, et al. Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J Infect Dis. 2014;210(11):1723–33.PubMedPubMedCentralCrossRef Brotman RM, Shardell MD, Gajer P, Tracy JK, Zenilman JM, Ravel J, et al. Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J Infect Dis. 2014;210(11):1723–33.PubMedPubMedCentralCrossRef
44.
go back to reference Shannon B, Yi T, Perusini S, Gajer P, Ma B, Humphrys M, et al. Association of HPV infection and clearance with cervicovaginal immunology and the vaginal microbiota. Mucosal Immunol. 2017;10(5):1310–9.PubMedPubMedCentralCrossRef Shannon B, Yi T, Perusini S, Gajer P, Ma B, Humphrys M, et al. Association of HPV infection and clearance with cervicovaginal immunology and the vaginal microbiota. Mucosal Immunol. 2017;10(5):1310–9.PubMedPubMedCentralCrossRef
45.
go back to reference Xu J, Peng J-J, Yang W, Fu K, Zhang Y. Vaginal microbiomes and ovarian cancer: a review. Am J Cancer Res. 2020;10(3):743.PubMedPubMedCentral Xu J, Peng J-J, Yang W, Fu K, Zhang Y. Vaginal microbiomes and ovarian cancer: a review. Am J Cancer Res. 2020;10(3):743.PubMedPubMedCentral
46.
go back to reference Leyva-Gómez G, Prado-Audelo D, María L, Ortega-Peña S, Mendoza-Muñoz N, Urbán-Morlán Z, et al. Modifications in vaginal microbiota and their influence on drug release: challenges and opportunities. Pharmaceutics. 2019;11(5):217.PubMedPubMedCentralCrossRef Leyva-Gómez G, Prado-Audelo D, María L, Ortega-Peña S, Mendoza-Muñoz N, Urbán-Morlán Z, et al. Modifications in vaginal microbiota and their influence on drug release: challenges and opportunities. Pharmaceutics. 2019;11(5):217.PubMedPubMedCentralCrossRef
47.
go back to reference Freitas AC, Hill JE. Quantification, isolation and characterization of Bifidobacterium from the vaginal microbiomes of reproductive aged women. Anaerobe. 2017;47:145–56.PubMedCrossRef Freitas AC, Hill JE. Quantification, isolation and characterization of Bifidobacterium from the vaginal microbiomes of reproductive aged women. Anaerobe. 2017;47:145–56.PubMedCrossRef
48.
go back to reference Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. Estrogen-gut microbiome axis: physiological and clinical implications. Maturitas. 2017;103:45–53.PubMedCrossRef Baker JM, Al-Nakkash L, Herbst-Kralovetz MM. Estrogen-gut microbiome axis: physiological and clinical implications. Maturitas. 2017;103:45–53.PubMedCrossRef
49.
go back to reference Kwa M, Plottel CS, Blaser MJ, Adams S. The intestinal microbiome and estrogen receptor–positive female breast cancer. JNCI 2016;108(8) Kwa M, Plottel CS, Blaser MJ, Adams S. The intestinal microbiome and estrogen receptor–positive female breast cancer. JNCI 2016;108(8)
50.
go back to reference De Seta F, Campisciano G, Zanotta N, Ricci G, Comar M. The vaginal community state types microbiome-immune network as key factor for bacterial vaginosis and aerobic vaginitis. Front Microbiol. 2019;10:2451.PubMedPubMedCentralCrossRef De Seta F, Campisciano G, Zanotta N, Ricci G, Comar M. The vaginal community state types microbiome-immune network as key factor for bacterial vaginosis and aerobic vaginitis. Front Microbiol. 2019;10:2451.PubMedPubMedCentralCrossRef
51.
52.
go back to reference Li H, Zang Y, Wang C, Li H, Fan A, Han C, et al. The interaction between microorganisms, metabolites, and immune system in the female genital tract microenvironment. Front Cell Infect Microbiol. 2020;10:796.CrossRef Li H, Zang Y, Wang C, Li H, Fan A, Han C, et al. The interaction between microorganisms, metabolites, and immune system in the female genital tract microenvironment. Front Cell Infect Microbiol. 2020;10:796.CrossRef
53.
go back to reference Nardis C, Mosca L, Mastromarino P. Vaginal microbiota and viral sexually transmitted diseases. Ann Ig. 2013;25(5):443–56.PubMed Nardis C, Mosca L, Mastromarino P. Vaginal microbiota and viral sexually transmitted diseases. Ann Ig. 2013;25(5):443–56.PubMed
54.
go back to reference Boris S, Barbés C. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect. 2000;2(5):543–6.PubMedCrossRef Boris S, Barbés C. Role played by lactobacilli in controlling the population of vaginal pathogens. Microbes Infect. 2000;2(5):543–6.PubMedCrossRef
55.
go back to reference Chan R, Reid G, Irvin R, Bruce A, Costerton J. Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments. Infect Immun. 1985;47(1):84–9.PubMedPubMedCentralCrossRef Chan R, Reid G, Irvin R, Bruce A, Costerton J. Competitive exclusion of uropathogens from human uroepithelial cells by Lactobacillus whole cells and cell wall fragments. Infect Immun. 1985;47(1):84–9.PubMedPubMedCentralCrossRef
56.
go back to reference Reid G, Cook RL, Bruce AW. Examination of strains of lactobacilli for properties that may influence bacterial interference in the urinary tract. J Urol. 1987;138(2):330–5.PubMedCrossRef Reid G, Cook RL, Bruce AW. Examination of strains of lactobacilli for properties that may influence bacterial interference in the urinary tract. J Urol. 1987;138(2):330–5.PubMedCrossRef
57.
go back to reference Ghadimi D, de Vrese M, Heller KJ, Schrezenmeir J. Lactic acid bacteria enhance autophagic ability of mononuclear phagocytes by increasing Th1 autophagy-promoting cytokine (IFN-γ) and nitric oxide (NO) levels and reducing Th2 autophagy-restraining cytokines (IL-4 and IL-13) in response to Mycobacterium tuberculosis antigen. Int Immunopharmacol. 2010;10(6):694–706.PubMedCrossRef Ghadimi D, de Vrese M, Heller KJ, Schrezenmeir J. Lactic acid bacteria enhance autophagic ability of mononuclear phagocytes by increasing Th1 autophagy-promoting cytokine (IFN-γ) and nitric oxide (NO) levels and reducing Th2 autophagy-restraining cytokines (IL-4 and IL-13) in response to Mycobacterium tuberculosis antigen. Int Immunopharmacol. 2010;10(6):694–706.PubMedCrossRef
59.
go back to reference Witkin SS, Mendes-Soares H, Linhares IM, Jayaram A, Ledger WJ, Forney LJ. Influence of vaginal bacteria and D-and L-lactic acid isomers on vaginal extracellular matrix metalloproteinase inducer: implications for protection against upper genital tract infections. MBio. 2013;4(4):e00460-e513.PubMedPubMedCentralCrossRef Witkin SS, Mendes-Soares H, Linhares IM, Jayaram A, Ledger WJ, Forney LJ. Influence of vaginal bacteria and D-and L-lactic acid isomers on vaginal extracellular matrix metalloproteinase inducer: implications for protection against upper genital tract infections. MBio. 2013;4(4):e00460-e513.PubMedPubMedCentralCrossRef
60.
go back to reference Nunn KL, Wang Y-Y, Harit D, Humphrys MS, Ma B, Cone R, et al. Enhanced trapping of HIV-1 by human cervicovaginal mucus is associated with Lactobacillus crispatus-dominant microbiota. MBio. 2015;6(5):e01084-e1115.PubMedPubMedCentralCrossRef Nunn KL, Wang Y-Y, Harit D, Humphrys MS, Ma B, Cone R, et al. Enhanced trapping of HIV-1 by human cervicovaginal mucus is associated with Lactobacillus crispatus-dominant microbiota. MBio. 2015;6(5):e01084-e1115.PubMedPubMedCentralCrossRef
61.
go back to reference Mitra A, MacIntyre DA, Marchesi JR, Lee YS, Bennett PR, Kyrgiou M. The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome. 2016;4(1):58.PubMedPubMedCentralCrossRef Mitra A, MacIntyre DA, Marchesi JR, Lee YS, Bennett PR, Kyrgiou M. The vaginal microbiota, human papillomavirus infection and cervical intraepithelial neoplasia: what do we know and where are we going next? Microbiome. 2016;4(1):58.PubMedPubMedCentralCrossRef
62.
go back to reference Audirac-Chalifour A, Torres-Poveda K, Bahena-Román M, Téllez-Sosa J, Martínez-Barnetche J, Cortina-Ceballos B, et al. Cervical microbiome and cytokine profile at various stages of cervical cancer: a pilot study. PLoS ONE. 2016;11(4): e0153274.PubMedPubMedCentralCrossRef Audirac-Chalifour A, Torres-Poveda K, Bahena-Román M, Téllez-Sosa J, Martínez-Barnetche J, Cortina-Ceballos B, et al. Cervical microbiome and cytokine profile at various stages of cervical cancer: a pilot study. PLoS ONE. 2016;11(4): e0153274.PubMedPubMedCentralCrossRef
63.
go back to reference Brotman RM, Shardell MD, Gajer P, Tracy JK, Zenilman JM, Ravel J, et al. Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J Infect Dis. 2014;210(11):1723–33.PubMedPubMedCentralCrossRef Brotman RM, Shardell MD, Gajer P, Tracy JK, Zenilman JM, Ravel J, et al. Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection. J Infect Dis. 2014;210(11):1723–33.PubMedPubMedCentralCrossRef
64.
go back to reference Macklaim JM, Fernandes AD, Di Bella JM, Hammond J-A, Reid G, Gloor GB. Comparative meta-RNA-seq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis. Microbiome. 2013;1(1):1–11.CrossRef Macklaim JM, Fernandes AD, Di Bella JM, Hammond J-A, Reid G, Gloor GB. Comparative meta-RNA-seq of the vaginal microbiota and differential expression by Lactobacillus iners in health and dysbiosis. Microbiome. 2013;1(1):1–11.CrossRef
65.
go back to reference Macklaim JM, Gloor GB, Anukam KC, Cribby S, Reid G. At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc Natl Acad Sci. 2011;108(Supplement 1):4688–95.PubMedCrossRef Macklaim JM, Gloor GB, Anukam KC, Cribby S, Reid G. At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc Natl Acad Sci. 2011;108(Supplement 1):4688–95.PubMedCrossRef
66.
67.
go back to reference Curty G, de Carvalho PS, Soares MA. The role of the cervicovaginal microbiome on the genesis and as a biomarker of premalignant cervical intraepithelial neoplasia and invasive cervical cancer. Int J Mol Sci. 2019; 21(1) Curty G, de Carvalho PS, Soares MA. The role of the cervicovaginal microbiome on the genesis and as a biomarker of premalignant cervical intraepithelial neoplasia and invasive cervical cancer. Int J Mol Sci. 2019; 21(1)
68.
go back to reference Di Paola M, Sani C, Clemente AM, Iossa A, Perissi E, Castronovo G, et al. Characterization of cervico-vaginal microbiota in women developing persistent high-risk Human Papillomavirus infection. Sci Rep. 2017;7(1):1–12.CrossRef Di Paola M, Sani C, Clemente AM, Iossa A, Perissi E, Castronovo G, et al. Characterization of cervico-vaginal microbiota in women developing persistent high-risk Human Papillomavirus infection. Sci Rep. 2017;7(1):1–12.CrossRef
69.
go back to reference Nowak RG, Randis TM, Desai P, He X, Robinson CK, Rath J, et al. Higher levels of a cytotoxic protein, vaginolysin, in Lactobacillus-deficient community state types at the vaginal mucosa. Sex Transm Dis. 2018;45(4): e14.PubMedPubMedCentralCrossRef Nowak RG, Randis TM, Desai P, He X, Robinson CK, Rath J, et al. Higher levels of a cytotoxic protein, vaginolysin, in Lactobacillus-deficient community state types at the vaginal mucosa. Sex Transm Dis. 2018;45(4): e14.PubMedPubMedCentralCrossRef
70.
go back to reference Tang J, Wu Y-M, Zhao P, Yang X-M, Jiang J-L, Chen Z-N. Overexpression of HAb18G/CD147 promotes invasion and metastasis via α3β1 integrin mediated FAK-paxillin and FAK-PI3K-Ca 2+ pathways. Cell Mol Life Sci. 2008;65(18):2933–42.PubMedPubMedCentralCrossRef Tang J, Wu Y-M, Zhao P, Yang X-M, Jiang J-L, Chen Z-N. Overexpression of HAb18G/CD147 promotes invasion and metastasis via α3β1 integrin mediated FAK-paxillin and FAK-PI3K-Ca 2+ pathways. Cell Mol Life Sci. 2008;65(18):2933–42.PubMedPubMedCentralCrossRef
71.
go back to reference Martino JL, Vermund SH. Vaginal douching: evidence for risks or benefits to women’s health. Epidemiol Rev. 2002;24(2):109–24.PubMedCrossRef Martino JL, Vermund SH. Vaginal douching: evidence for risks or benefits to women’s health. Epidemiol Rev. 2002;24(2):109–24.PubMedCrossRef
72.
go back to reference Anahtar MN, Byrne EH, Doherty KE, Bowman BA, Yamamoto HS, Soumillon M, et al. Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity. 2015;42(5):965–76.PubMedPubMedCentralCrossRef Anahtar MN, Byrne EH, Doherty KE, Bowman BA, Yamamoto HS, Soumillon M, et al. Cervicovaginal bacteria are a major modulator of host inflammatory responses in the female genital tract. Immunity. 2015;42(5):965–76.PubMedPubMedCentralCrossRef
73.
go back to reference Chee WJY, Chew SY, Than LTL. Vaginal microbiota and the potential of Lactobacillus derivatives in maintaining vaginal health. Microb Cell Fact. 2020;19(1):1–24.CrossRef Chee WJY, Chew SY, Than LTL. Vaginal microbiota and the potential of Lactobacillus derivatives in maintaining vaginal health. Microb Cell Fact. 2020;19(1):1–24.CrossRef
74.
go back to reference Brotman RM, Shardell MD, Gajer P, Fadrosh D, Chang K, Silver M, et al. Association between the vaginal microbiota, menopause status and signs of vulvovaginal atrophy. Menopause (New York, NY). 2014;21(5):450.CrossRef Brotman RM, Shardell MD, Gajer P, Fadrosh D, Chang K, Silver M, et al. Association between the vaginal microbiota, menopause status and signs of vulvovaginal atrophy. Menopause (New York, NY). 2014;21(5):450.CrossRef
75.
go back to reference Fethers KA, Fairley CK, Hocking JS, Gurrin LC, Bradshaw CS. Sexual risk factors and bacterial vaginosis: a systematic review and meta-analysis. Clin Infect Dis. 2008;47(11):1426–35.PubMedCrossRef Fethers KA, Fairley CK, Hocking JS, Gurrin LC, Bradshaw CS. Sexual risk factors and bacterial vaginosis: a systematic review and meta-analysis. Clin Infect Dis. 2008;47(11):1426–35.PubMedCrossRef
76.
go back to reference Gosmann C, Anahtar MN, Handley SA, Farcasanu M, Abu-Ali G, Bowman BA, et al. Lactobacillus-deficient cervicovaginal bacterial communities are associated with increased HIV acquisition in young South African women. Immunity. 2017;46(1):29–37.PubMedPubMedCentralCrossRef Gosmann C, Anahtar MN, Handley SA, Farcasanu M, Abu-Ali G, Bowman BA, et al. Lactobacillus-deficient cervicovaginal bacterial communities are associated with increased HIV acquisition in young South African women. Immunity. 2017;46(1):29–37.PubMedPubMedCentralCrossRef
77.
go back to reference Shannon B, Gajer P, Yi T, Ma B, Humphrys M, Thomas-Pavanel J, et al. Distinct effects of the cervicovaginal microbiota and herpes simplex type 2 infection on female genital tract immunology. J Infect Dis. 2017;215(9):1366–75.PubMedPubMedCentralCrossRef Shannon B, Gajer P, Yi T, Ma B, Humphrys M, Thomas-Pavanel J, et al. Distinct effects of the cervicovaginal microbiota and herpes simplex type 2 infection on female genital tract immunology. J Infect Dis. 2017;215(9):1366–75.PubMedPubMedCentralCrossRef
78.
go back to reference Wylie KM, Mihindukulasuriya KA, Zhou Y, Sodergren E, Storch GA, Weinstock GM. Metagenomic analysis of double-stranded DNA viruses in healthy adults. BMC Biol. 2014;12(1):1–10.CrossRef Wylie KM, Mihindukulasuriya KA, Zhou Y, Sodergren E, Storch GA, Weinstock GM. Metagenomic analysis of double-stranded DNA viruses in healthy adults. BMC Biol. 2014;12(1):1–10.CrossRef
79.
go back to reference Santella B, Schettino MT, Franci G, De Franciscis P, Colacurci N, Schiattarella A, et al. Microbiota and HPV: the role of viral infection on vaginal microbiota. J Med Virol. 2022;94(9):4478–84.PubMedPubMedCentralCrossRef Santella B, Schettino MT, Franci G, De Franciscis P, Colacurci N, Schiattarella A, et al. Microbiota and HPV: the role of viral infection on vaginal microbiota. J Med Virol. 2022;94(9):4478–84.PubMedPubMedCentralCrossRef
80.
go back to reference Kwon M, Seo SS, Kim MK, Lee DO, Lim MC. Compositional and functional differences between microbiota and cervical carcinogenesis as identified by shotgun metagenomic sequencing. Cancers (Basel). 2019; 11(3) Kwon M, Seo SS, Kim MK, Lee DO, Lim MC. Compositional and functional differences between microbiota and cervical carcinogenesis as identified by shotgun metagenomic sequencing. Cancers (Basel). 2019; 11(3)
81.
go back to reference Pybus V, Onderdonk AB. Evidence for a commensal, symbiotic relationship between Gardnerella vaginalis and Prevotella bivia involving ammonia: potential significance for bacterial vaginosis. J Infect Dis. 1997;175(2):406–13.PubMedCrossRef Pybus V, Onderdonk AB. Evidence for a commensal, symbiotic relationship between Gardnerella vaginalis and Prevotella bivia involving ammonia: potential significance for bacterial vaginosis. J Infect Dis. 1997;175(2):406–13.PubMedCrossRef
82.
go back to reference Pybus V, Onderdonk AB. A commensal symbiosis between Prevotella bivia and Peptostreptococcus anaerobius involves amino acids: potential significance to the pathogenesis of bacterial vaginosis. FEMS Immunol Med Microbiol. 1998;22(4):317–27.PubMedCrossRef Pybus V, Onderdonk AB. A commensal symbiosis between Prevotella bivia and Peptostreptococcus anaerobius involves amino acids: potential significance to the pathogenesis of bacterial vaginosis. FEMS Immunol Med Microbiol. 1998;22(4):317–27.PubMedCrossRef
83.
go back to reference Lee JE, Lee S, Lee H, Song Y-M, Lee K, Han MJ, et al. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS ONE. 2013;8(5): e63514.PubMedPubMedCentralCrossRef Lee JE, Lee S, Lee H, Song Y-M, Lee K, Han MJ, et al. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS ONE. 2013;8(5): e63514.PubMedPubMedCentralCrossRef
84.
go back to reference Lee JE, Lee S, Lee H, Song YM, Lee K, Han MJ, et al. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS ONE. 2013;8(5): e63514.PubMedPubMedCentralCrossRef Lee JE, Lee S, Lee H, Song YM, Lee K, Han MJ, et al. Association of the vaginal microbiota with human papillomavirus infection in a Korean twin cohort. PLoS ONE. 2013;8(5): e63514.PubMedPubMedCentralCrossRef
85.
go back to reference Łaniewski P, Barnes D, Goulder A, Cui H, Roe DJ, Chase DM, et al. Linking cervicovaginal immune signatures, HPV and microbiota composition in cervical carcinogenesis in non-Hispanic and Hispanic women. Sci Rep. 2018;8(1):7593.PubMedPubMedCentralCrossRef Łaniewski P, Barnes D, Goulder A, Cui H, Roe DJ, Chase DM, et al. Linking cervicovaginal immune signatures, HPV and microbiota composition in cervical carcinogenesis in non-Hispanic and Hispanic women. Sci Rep. 2018;8(1):7593.PubMedPubMedCentralCrossRef
86.
go back to reference Mitra A, MacIntyre DA, Lee YS, Smith A, Marchesi JR, Lehne B, et al. Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci Rep. 2015;5(1):16865.PubMedPubMedCentralCrossRef Mitra A, MacIntyre DA, Lee YS, Smith A, Marchesi JR, Lehne B, et al. Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity. Sci Rep. 2015;5(1):16865.PubMedPubMedCentralCrossRef
87.
go back to reference Borgogna JC, Shardell MD, Santori EK, Nelson TM, Rath JM, Glover ED, et al. The vaginal metabolome and microbiota of cervical HPV-positive and HPV-negative women: a cross-sectional analysis. BJOG. 2020;127(2):182–92.PubMedCrossRef Borgogna JC, Shardell MD, Santori EK, Nelson TM, Rath JM, Glover ED, et al. The vaginal metabolome and microbiota of cervical HPV-positive and HPV-negative women: a cross-sectional analysis. BJOG. 2020;127(2):182–92.PubMedCrossRef
88.
go back to reference Ilhan ZE, Łaniewski P, Thomas N, Roe DJ, Chase DM, Herbst-Kralovetz MM. Deciphering the complex interplay between microbiota, HPV, inflammation and cancer through cervicovaginal metabolic profiling. EBioMedicine. 2019;44:675–90.PubMedPubMedCentralCrossRef Ilhan ZE, Łaniewski P, Thomas N, Roe DJ, Chase DM, Herbst-Kralovetz MM. Deciphering the complex interplay between microbiota, HPV, inflammation and cancer through cervicovaginal metabolic profiling. EBioMedicine. 2019;44:675–90.PubMedPubMedCentralCrossRef
89.
go back to reference Schmitt A, Harry J, Rapp B, Wettstein F, Iftner T. Comparison of the properties of the E6 and E7 genes of low-and high-risk cutaneous papillomaviruses reveals strongly transforming and high Rb-binding activity for the E7 protein of the low-risk human papillomavirus type 1. J Virol. 1994;68(11):7051–9.PubMedPubMedCentralCrossRef Schmitt A, Harry J, Rapp B, Wettstein F, Iftner T. Comparison of the properties of the E6 and E7 genes of low-and high-risk cutaneous papillomaviruses reveals strongly transforming and high Rb-binding activity for the E7 protein of the low-risk human papillomavirus type 1. J Virol. 1994;68(11):7051–9.PubMedPubMedCentralCrossRef
90.
go back to reference Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer. 2007;7(1):11–22.PubMedCrossRef Woodman CB, Collins SI, Young LS. The natural history of cervical HPV infection: unresolved issues. Nat Rev Cancer. 2007;7(1):11–22.PubMedCrossRef
92.
go back to reference Doerflinger SY, Throop AL, 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. 2014;209(12):1989–99.PubMedCrossRef Doerflinger SY, Throop AL, 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. 2014;209(12):1989–99.PubMedCrossRef
93.
go back to reference Libby EK, Pascal KE, Mordechai E, Adelson ME, Trama JP. Atopobium vaginae triggers an innate immune response in an in vitro model of bacterial vaginosis. Microbes Infect. 2008;10(4):439–46.PubMedCrossRef Libby EK, Pascal KE, Mordechai E, Adelson ME, Trama JP. Atopobium vaginae triggers an innate immune response in an in vitro model of bacterial vaginosis. Microbes Infect. 2008;10(4):439–46.PubMedCrossRef
94.
go back to reference Libertucci J, Young VB. The role of the microbiota in infectious diseases. Nat Microbiol. 2019;4(1):35–45.PubMedCrossRef Libertucci J, Young VB. The role of the microbiota in infectious diseases. Nat Microbiol. 2019;4(1):35–45.PubMedCrossRef
95.
go back to reference Anderson BL, Cu-uvin S, Raker CA, Fitzsimmons C, Hillier SL. Subtle perturbations of genital microflora alter mucosal immunity among low-risk pregnant women. Acta Obstet Gynecol Scand. 2011;90(5):510–5.PubMedCrossRef Anderson BL, Cu-uvin S, Raker CA, Fitzsimmons C, Hillier SL. Subtle perturbations of genital microflora alter mucosal immunity among low-risk pregnant women. Acta Obstet Gynecol Scand. 2011;90(5):510–5.PubMedCrossRef
96.
go back to reference Hedge SR, Barrientes F, Desmond RA, Schwebke JR. Local and systemic cytokine levels in relation to changes in vaginal flora. J Infect Dis. 2006;193(4):556–62.CrossRef Hedge SR, Barrientes F, Desmond RA, Schwebke JR. Local and systemic cytokine levels in relation to changes in vaginal flora. J Infect Dis. 2006;193(4):556–62.CrossRef
97.
go back to reference Motevaseli E, Shirzad M, Akrami SM, Mousavi A-S, Mirsalehian A, Modarressi MH. Normal and tumour cervical cells respond differently to vaginal lactobacilli, independent of pH and lactate. J Med Microbiol. 2013;62(7):1065–72.PubMedCrossRef Motevaseli E, Shirzad M, Akrami SM, Mousavi A-S, Mirsalehian A, Modarressi MH. Normal and tumour cervical cells respond differently to vaginal lactobacilli, independent of pH and lactate. J Med Microbiol. 2013;62(7):1065–72.PubMedCrossRef
98.
go back to reference Borgdorff H, Gautam R, Armstrong SD, Xia D, Ndayisaba GF, van Teijlingen NH, et al. Cervicovaginal microbiome dysbiosis is associated with proteome changes related to alterations of the cervicovaginal mucosal barrier. Mucosal Immunol. 2016;9(3):621–33.PubMedCrossRef Borgdorff H, Gautam R, Armstrong SD, Xia D, Ndayisaba GF, van Teijlingen NH, et al. Cervicovaginal microbiome dysbiosis is associated with proteome changes related to alterations of the cervicovaginal mucosal barrier. Mucosal Immunol. 2016;9(3):621–33.PubMedCrossRef
99.
go back to reference Üren A, Fallen S, Yuan H, Usubütün A, Küçükali T, Schlegel R, et al. Activation of the canonical Wnt pathway during genital keratinocyte transformation: a model for cervical cancer progression. Can Res. 2005;65(14):6199–206.CrossRef Üren A, Fallen S, Yuan H, Usubütün A, Küçükali T, Schlegel R, et al. Activation of the canonical Wnt pathway during genital keratinocyte transformation: a model for cervical cancer progression. Can Res. 2005;65(14):6199–206.CrossRef
101.
go back to reference López-Moreno A, Aguilera M. Vaginal probiotics for reproductive health and related dysbiosis: systematic review and meta-analysis. J Clin Med. 2021;10(7):1461.PubMedPubMedCentralCrossRef López-Moreno A, Aguilera M. Vaginal probiotics for reproductive health and related dysbiosis: systematic review and meta-analysis. J Clin Med. 2021;10(7):1461.PubMedPubMedCentralCrossRef
102.
go back to reference Machado D, Castro J, Palmeira-de-Oliveira A, Martinez-de-Oliveira J, Cerca N. Bacterial vaginosis biofilms: challenges to current therapies and emerging solutions. Front Microbiol. 2016;6:1528.PubMedPubMedCentralCrossRef Machado D, Castro J, Palmeira-de-Oliveira A, Martinez-de-Oliveira J, Cerca N. Bacterial vaginosis biofilms: challenges to current therapies and emerging solutions. Front Microbiol. 2016;6:1528.PubMedPubMedCentralCrossRef
103.
go back to reference Ebner S, Smug LN, Kneifel W, Salminen SJ, Sanders ME. Probiotics in dietary guidelines and clinical recommendations outside the European Union. World J Gastroenterol: WJG. 2014;20(43):16095.PubMedPubMedCentralCrossRef Ebner S, Smug LN, Kneifel W, Salminen SJ, Sanders ME. Probiotics in dietary guidelines and clinical recommendations outside the European Union. World J Gastroenterol: WJG. 2014;20(43):16095.PubMedPubMedCentralCrossRef
104.
go back to reference Verhoeven V, Renard N, Makar A, Van Royen P, Bogers J-P, Lardon F, et al. Probiotics enhance the clearance of human papillomavirus-related cervical lesions: a prospective controlled pilot study. Eur J Cancer Prev. 2013;22(1):46–51.PubMedCrossRef Verhoeven V, Renard N, Makar A, Van Royen P, Bogers J-P, Lardon F, et al. Probiotics enhance the clearance of human papillomavirus-related cervical lesions: a prospective controlled pilot study. Eur J Cancer Prev. 2013;22(1):46–51.PubMedCrossRef
105.
go back to reference Palma E, Recine N, Domenici L, Giorgini M, Pierangeli A, Panici PB. Long-term Lactobacillus rhamnosus BMX 54 application to restore a balanced vaginal ecosystem: a promising solution against HPV-infection. BMC Infect Dis. 2018;18(1):1–7.CrossRef Palma E, Recine N, Domenici L, Giorgini M, Pierangeli A, Panici PB. Long-term Lactobacillus rhamnosus BMX 54 application to restore a balanced vaginal ecosystem: a promising solution against HPV-infection. BMC Infect Dis. 2018;18(1):1–7.CrossRef
106.
go back to reference Cha M-K, Lee D-K, An H-M, Lee S-W, Shin S-H, Kwon J-H, et al. Antiviral activity of Bifidobacterium adolescentis SPM1005-A on human papillomavirus type 16. BMC Med. 2012;10(1):1–6.CrossRef Cha M-K, Lee D-K, An H-M, Lee S-W, Shin S-H, Kwon J-H, et al. Antiviral activity of Bifidobacterium adolescentis SPM1005-A on human papillomavirus type 16. BMC Med. 2012;10(1):1–6.CrossRef
107.
go back to reference Collins SL, McMillan A, Seney S, van der Veer C, Kort R, Sumarah MW, et al. Promising prebiotic candidate established by evaluation of lactitol, lactulose, raffinose, and oligofructose for maintenance of a lactobacillus-dominated vaginal microbiota. Appl Environ Microbiol. 2018;84(5):e02200-e2217.PubMedPubMedCentralCrossRef Collins SL, McMillan A, Seney S, van der Veer C, Kort R, Sumarah MW, et al. Promising prebiotic candidate established by evaluation of lactitol, lactulose, raffinose, and oligofructose for maintenance of a lactobacillus-dominated vaginal microbiota. Appl Environ Microbiol. 2018;84(5):e02200-e2217.PubMedPubMedCentralCrossRef
108.
go back to reference Coste I, Judlin P, Lepargneur J-P, Bou-Antoun S. Safety and efficacy of an intravaginal prebiotic gel in the prevention of recurrent bacterial vaginosis: a randomized double-blind study. Obstet Gynecol Int. 2012;2012. Coste I, Judlin P, Lepargneur J-P, Bou-Antoun S. Safety and efficacy of an intravaginal prebiotic gel in the prevention of recurrent bacterial vaginosis: a randomized double-blind study. Obstet Gynecol Int. 2012;2012.
109.
go back to reference Tester R, Al-Ghazzewi F, Shen N, Chen Z, Chen F, Yang J, et al. The use of konjac glucomannan hydrolysates to recover healthy microbiota in infected vaginas treated with an antifungal agent. Beneficial Microbes. 2012;3(1):61–6.PubMedCrossRef Tester R, Al-Ghazzewi F, Shen N, Chen Z, Chen F, Yang J, et al. The use of konjac glucomannan hydrolysates to recover healthy microbiota in infected vaginas treated with an antifungal agent. Beneficial Microbes. 2012;3(1):61–6.PubMedCrossRef
110.
go back to reference Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.PubMedCrossRef Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–86.PubMedCrossRef
111.
go back to reference Lev-Sagie A, Goldman-Wohl D, Cohen Y, Dori-Bachash M, Leshem A, Mor U, et al. Vaginal microbiome transplantation in women with intractable bacterial vaginosis. Nat Med. 2019;25(10):1500–4.PubMedCrossRef Lev-Sagie A, Goldman-Wohl D, Cohen Y, Dori-Bachash M, Leshem A, Mor U, et al. Vaginal microbiome transplantation in women with intractable bacterial vaginosis. Nat Med. 2019;25(10):1500–4.PubMedCrossRef
112.
go back to reference Ma D, Chen Y, Chen T. Vaginal microbiota transplantation for the treatment of bacterial vaginosis: a conceptual analysis. FEMS Microbiol Lett. 2019;366(4):fnz025. Ma D, Chen Y, Chen T. Vaginal microbiota transplantation for the treatment of bacterial vaginosis: a conceptual analysis. FEMS Microbiol Lett. 2019;366(4):fnz025.
113.
go back to reference DeLong K, Bensouda S, Zulfiqar F, Zierden HC, Hoang TM, Abraham AG, et al. Conceptual design of a universal donor screening approach for vaginal microbiota transplant. Front Cell Infect Microbiol. 2019;9:306.PubMedPubMedCentralCrossRef DeLong K, Bensouda S, Zulfiqar F, Zierden HC, Hoang TM, Abraham AG, et al. Conceptual design of a universal donor screening approach for vaginal microbiota transplant. Front Cell Infect Microbiol. 2019;9:306.PubMedPubMedCentralCrossRef
Metadata
Title
The interplay between human papillomavirus and vaginal microbiota in cervical cancer development
Authors
Kimia Sharifian
Zabihollah Shoja
Somayeh Jalilvand
Publication date
01-12-2023
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2023
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-023-02037-8

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