Cervical intraepithelial neoplasia disease progression is associated with increased vaginal microbiome diversity
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Persistent infection with oncogenic Human Papillomavirus (HPV) is necessary for cervical carcinogenesis. Although evidence suggests that the vaginal microbiome plays a functional role in the persistence or regression of HPV infections, this has yet to be described in women with cervical intra-epithelial neoplasia (CIN). We hypothesised that increasing microbiome diversity is associated with increasing CIN severity. llumina MiSeq sequencing of 16S rRNA gene amplicons was used to characterise the vaginal microbiota of women with low-grade squamous intra-epithelial lesions (LSIL; n = 52), high-grade (HSIL; n = 92), invasive cervical cancer (ICC; n = 5) and healthy controls (n = 20). Hierarchical clustering analysis revealed an increased prevalence of microbiomes characterised by high-diversity and low levels of Lactobacillus spp. (community state type-CST IV) with increasing disease severity, irrespective of HPV status (Normal = 2/20,10%; LSIL = 11/52,21%; HSIL = 25/92,27%; ICC = 2/5,40%). Increasing disease severity was associated with decreasing relative abundance of Lactobacillus spp. The vaginal microbiome in HSIL was characterised by higher levels of Sneathia sanguinegens (P < 0.01), Anaerococcus tetradius (P < 0.05) and Peptostreptococcus anaerobius (P < 0.05) and lower levels of Lactobacillus jensenii (P < 0.01) compared to LSIL. Our results suggest advancing CIN disease severity is associated with increasing vaginal microbiota diversity and may be involved in regulating viral persistence and disease progression.
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CSTs III and IV are frequently linked with presence of HPV infection and development of preinvasive cervical disease states.
“Recent observational cross-sectional studies support the concept that CSTs III and IV, in particular, are frequently linked with the presence of HPV infection and development of preinvasive cervical disease states (Lee J.E. et al., 2013; Brotman et al., 2014; Mitra et al., 2015).”
From Viral Infections, the Microbiome, and Probiotics (2021) · cites this paper as Mitra et al., 2015
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Search and clustering orders of magnitude faster than BLAST
Edgar, R. C. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq461 · Cited by 20,617 · see citing works
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
Wang, Q., Garrity, G. M., Tiedje, J. M., & Cole, J. R. (2007) · Applied and Environmental Microbiology · doi:10.1128/aem.00062-07 · Cited by 19,946 · see citing works
Coussens, L. M., & Werb, Z. (2002) · Nature · doi:10.1038/nature01322 · Cited by 15,111 · see citing works
Kozich, J. J., Westcott, S. L., Baxter, N. T., Highlander, S. K., & Schloss, P. D. (2013) · Applied and Environmental Microbiology · doi:10.1128/aem.01043-13 · Cited by 7,004 · see citing works
Vaginal microbiome of reproductive-age women
Ravel, J., Gajer, P., Abdo, Z., Schneider, G. M., Koenig, S. S. K., McCulle, S. L., Karlebach, S., Gorle, R., Russell, J., Tacket, C. O., et al. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1002611107 · Cited by 4,254 · see citing works
Kostic, A. D., Chun, E., Robertson, L., Glickman, J. N., Gallini, C. A., Michaud, M., Clancy, T. E., Chung, D. C., Lochhead, P., Hold, G. L., et al. (2013) · Cell Host & Microbe · doi:10.1016/j.chom.2013.07.007 · Cited by 2,718 · see citing works
The Intestinal Microbiota Modulates the Anticancer Immune Effects of Cyclophosphamide
Viaud, S., Saccheri, F., Mignot, G., Yamazaki, T., Daillère, R., Hannani, D., Enot, D. P., Pfirschke, C., Engblom, C., Pittet, M. J., et al. (2013) · Science · doi:10.1126/science.1240537 · Cited by 2,050 · see citing works
Genomic analysis identifies association of <i>Fusobacterium</i> with colorectal carcinoma
Kostic, A. D., Gevers, D., Pedamallu, C. S., Michaud, M., Duke, F., Earl, A. M., Ojesina, A. I., Jung, J., Bass, A. J., Tabernero, J., et al. (2012) · Genome Research · doi:10.1101/gr.126573.111 · Cited by 1,960 · see citing works
Temporal Dynamics of the Human Vaginal Microbiota
Gajer, P., Brotman, R. M., Bai, G., Sakamoto, J. M., Schütte, U. M. E., Zhong, X., Koenig, S. S. K., Fu, L., Ma, Z. S., Zhou, X., et al. (2012) · Science Translational Medicine · doi:10.1126/scitranslmed.3003605 · Cited by 1,551 · see citing works
Kyrgiou, M., Koliopoulos, G., Martin-Hirsch, P., Arbyn, M., Prendiville, W., & Paraskevaidis, E. (2006) · The Lancet · doi:10.1016/s0140-6736(06)68181-6 · Cited by 1,120 · see citing works
Identifying biologically relevant differences between metagenomic communities
Parks, D. H., & Beiko, R. G. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btq041 · Cited by 942 · see citing works
Romero, R., Hassan, S. S., Gajer, P., Tarca, A. L., Fadrosh, D. W., Nikita, L., Galuppi, M., Lamont, R. F., Chaemsaithong, P., Miranda, J., et al. (2014) · Microbiome · doi:10.1186/2049-2618-2-4 · Cited by 852 · see citing works
Systematic review and meta-analysis of psychological therapies for children with chronic pain
Fisher, E., Heathcote, L., Palermo, T. M., de C Williams, A. C., Lau, J., & Eccleston, C. (2014) · Journal of Pediatric Psychology · doi:10.1093/jpepsy/jsu008 · Cited by 710 · see citing works
Bacterial vaginosis and HIV acquisition: A meta-analysis of published studies
Atashili, J., Poole, C., Ndumbe, P. M., Adimora, A. A., & Smith, J. S. (2008) · AIDS · doi:10.1097/qad.0b013e3283021a37 · Cited by 706 · see citing works
Human papillomavirus and cancer: the epidemiological evidence
Muñóz, N. (2000) · Journal of Clinical Virology · doi:10.1016/s1386-6532(00)00125-6 · Cited by 597 · see citing works
The vaginal microbiome during pregnancy and the postpartum period in a European population
MacIntyre, D. A., Chandiramani, M., Lee, Y. S., Kindinger, L. M., Smith, A., Angelopoulos, N., Lehne, B. C., Arulkumaran, S., Brown, R., Teoh, T. G., et al. (2015) · Scientific Reports · doi:10.1038/srep08988 · Cited by 565 · see citing works
Towards the Human Colorectal Cancer Microbiome
Marchesi, J. R., Dutilh, B. E., Hall, N., Peters, W. H. M., Roelofs, R., Boleij, A., & Tjalsma, H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020447 · Cited by 552 · see citing works
Boskey, E. R., Cone, R. A., Whaley, K. J., & Moench, T. R. (2001) · Human Reproduction · doi:10.1093/humrep/16.9.1809 · Cited by 500 · see citing works
Myers, E. R., McCrory, D. C., Nanda, K., Bastian, L., & Matchar, D. B. (2000) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a010166 · Cited by 470 · see citing works
Role played by lactobacilli in controlling the population of vaginal pathogens
Boris, S., & Barbés, C. (2000) · Microbes and Infection · doi:10.1016/s1286-4579(00)00313-0 · Cited by 430 · see citing works
Defense factors of vaginal lactobacilli
Aroutcheva, A. A., Gariti, D., Simon, M., Shott, S., Faro, J. P., Simoes, J. A., Gurguis, A., & Faro, S. (2001) · American Journal of Obstetrics and Gynecology · doi:10.1067/mob.2001.115867 · Cited by 426 · see citing works
Control of the Microbial Flora of the Vagina by H202-Generating Lactobacilli
Klebanoff, S. J., Hillier, S. L., Eschenbach, D. A., & Waltersdorph, A. M. (1991) · The Journal of Infectious Diseases · doi:10.1093/infdis/164.1.94 · Cited by 420 · see citing works
Brotman, R. M., Klebanoff, M. A., Nansel, T. R., Yu, K. F., Andrews, W. W., Zhang, J., & Schwebke, J. R. (2010) · The Journal of Infectious Diseases · doi:10.1086/657320 · Cited by 416 · see citing works
Interplay between the temporal dynamics of the vaginal microbiota and human papillomavirus detection
Brotman, R. M., Shardell, M. D., Gajer, P., Tracy, J. K., Zenilman, J. M., Ravel, J., & Gravitt, P. E. (2014) · Journal of Infectious Diseases · doi:10.1093/infdis/jiu330 · Cited by 411 · see citing works
The natural history of type-specific human papillomavirus infections in female university students.
Richardson, H., Kelsall, G., Tellier, P., Voyer, H., Abrahamowicz, M., Ferenczy, A. S., Coutlée, F., & Franco, E. L. (2003) · PubMed · Cited by 403 · see citing works
Gillet, E., Meys, J. F., Verstraelen, H., Bosire, C., De Sutter, P., Temmerman, M., & Broeck, D. V. (2011) · BMC Infectious Diseases · doi:10.1186/1471-2334-11-10 · Cited by 354 · see citing works
Association of the Vaginal Microbiota with Human Papillomavirus Infection in a Korean Twin Cohort
Lee, J. E., Lee, S., Lee, H., Song, Y., Lee, K., Han, M. J., Sung, J., & Ko, G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0063514 · Cited by 339 · see citing works
Klebanoff, S. J., & Coombs, R. W. (1991) · The Journal of Experimental Medicine · doi:10.1084/jem.174.1.289 · Cited by 273 · see citing works
The Microbiota of the Vagina and Its Influence on Women’s Health and Disease
Martin, D. H. (2011) · The American Journal of the Medical Sciences · doi:10.1097/maj.0b013e31823ea228 · Cited by 243 · see citing works
Systematic Review and Metaanalysis
Shimada, T., Noguchi, Y., Jackson, J. L., Miyashita, J., Hayashino, Y., Kamiya, T., Yamazaki, S., Matsumura, T., & Fukuhara, S. (2009) · CHEST Journal · doi:10.1378/chest.08-2602 · Cited by 239 · see citing works
Gillet, E., Meys, J., Verstraelen, H., Verhelst, R., Sutter, P. D., Temmerman, M., & Broeck, D. V. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045201 · Cited by 203 · see citing works
Kyrgiou, M., Mitra, A., Arbyn, M., Stasinou, S. M., Martin-Hirsch, P., Bennett, P., & Paraskevaidis, E. (2014) · BMJ · doi:10.1136/bmj.g6192 · Cited by 188 · see citing works
Viral Infection of the Pregnant Cervix Predisposes to Ascending Bacterial Infection
Racicot, K. E., Cardenas, I., Wünsche, V., Aldo, P. B., Guller, S. M., Means, R. E., Romero, R. J., & Mor, G. (2013) · The Journal of Immunology · doi:10.4049/jimmunol.1300661 · Cited by 186 · see citing works
Ocaña, V. S., Holgado, A. A. P. D. R., & Nader-Macı́as, M. E. (1999) · Applied and Environmental Microbiology · doi:10.1128/aem.65.12.5631-5635.1999 · Cited by 171 · see citing works
Association between cigarette smoking and the vaginal microbiota: a pilot study
Brotman, R. M., He, X., Gajer, P., Fadrosh, D., Sharma, E., Mongodin, E. F., Ravel, J., Glover, E. D., & Rath, J. M. (2014) · BMC Infectious Diseases · doi:10.1186/1471-2334-14-471 · Cited by 170 · see citing works
Vaginal Microflora in Postmenopausal Women Who Have Not Received Estrogen Replacement Therapy
Hillier, S. L., & Lau, R. J. (1997) · Clinical Infectious Diseases · doi:10.1086/516221 · Cited by 168 · see citing works
Vujic, G., Jajac Knez, A., Despot Stefanovic, V., & Kuzmic Vrbanovic, V. (2013) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2012.12.031 · Cited by 159 · see citing works
Disruption of urogenital biofilms by lactobacilli
McMillan, A., Dell, M., Zellar, M. P., Cribby, S., Martz, S., Hong, E., Fu, J. M., Abbas, A., Dang, T., Miller, W., et al. (2011) · Colloids and Surfaces B Biointerfaces · doi:10.1016/j.colsurfb.2011.03.016 · Cited by 156 · see citing works
Clark, R. A., & Klebanoff, S. J. (1979) · The Journal of Immunology · doi:10.4049/jimmunol.122.6.2605 · Cited by 143 · see citing works
Th1 Cytokine Patterns in Cervical Human Papillomavirus Infection
Scott, M. E., Stites, D. P., & Moscicki, A. (1999) · Clinical and Diagnostic Laboratory Immunology · doi:10.1128/cdli.6.5.751-755.1999 · Cited by 136 · see citing works
Motevaseli, E., Shirzad, ., Akrami, S. M., Mousavi, A., Mirsalehian, A., & Modarressi, M. H. (2013) · Journal of Medical Microbiology · doi:10.1099/jmm.0.057521-0 · Cited by 134 · see citing works
Bacterial Vaginosis and the Natural History of Human Papillomavirus
King, C. C., Jamieson, D. J., Wiener, J. B., Cu‐Uvin, S., Klein, R. S., Rompalo, A. M., Shah, K. V., & Sobel, J. D. (2011) · Infectious Diseases in Obstetrics and Gynecology · doi:10.1155/2011/319460 · Cited by 121 · see citing works
Role of inflammation in pancreatic carcinogenesis and the implications for future therapy
Garcea, G., Dennison, A. R., Steward, W. P., & Berry, D. P. (2005) · Pancreatology · doi:10.1159/000087493 · Cited by 117 · see citing works
Bacterial vaginosis is conducive to the persistence of HPV infection
Guo, Y.-L., You, K., Qiao, J., Zhao, Y.-M., & Geng, L. (2012) · International Journal of STD & AIDS · doi:10.1258/ijsa.2012.011342 · Cited by 116 · see citing works
Woodworth, C. D. (2002) · Frontiers in bioscience · doi:10.2741/a898 · Cited by 81 · see citing works
Hesselink, A. T., Meijer, C. J. L. M., Poljak, M., Berkhof, J. H., van Kemenade, F. J., van der Salm, M. L., Bogaarts, M., Snijders, P. J. F., & Heideman, D. A. M. (2013) · Journal of Clinical Microbiology · doi:10.1128/jcm.00633-13 · Cited by 53 · see citing works
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Lloyd-Price, J., Abu-Ali, G., & Huttenhower, C. (2016) · Genome Medicine · doi:10.1186/s13073-016-0307-y · Cited by 1,891 · see citing works
The Vaginal Microenvironment: The Physiologic Role of Lactobacilli
Amabebe, E., & Anumba, D. O. C. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00181 · Cited by 785 · see citing works
Anticancer effects of the microbiome and its products
Zitvogel, L., Daillère, R., Roberti, M. P., Routy, B., & Kroemer, G. (2017) · Nature Reviews Microbiology · doi:10.1038/nrmicro.2017.44 · Cited by 538 · see citing works
Mitra, A., MacIntyre, D. A., Marchesi, J. R., Lee, Y. S., Bennett, P. R., & Kyrgiou, M. (2016) · Microbiome · doi:10.1186/s40168-016-0203-0 · Cited by 484 · see citing works
The HPV E6/E7 Oncogenes: Key Factors for Viral Carcinogenesis and Therapeutic Targets
Hoppe‐Seyler, K., Bossler, F., Braun, J. A., Herrmann, A. L., & Hoppe‐Seyler, F. (2017) · Trends in Microbiology · doi:10.1016/j.tim.2017.07.007 · Cited by 464 · see citing works
The microbiome and gynaecological cancer development, prevention and therapy
Łaniewski, P., Ilhan, Z. E., & Herbst‐Kralovetz, M. M. (2020) · Nature Reviews Urology · doi:10.1038/s41585-020-0286-z · Cited by 469 · see citing works
Tainio, K., Athanasiou, A., Tikkinen, K. A. O., Aaltonen, R. L., Cárdenas, J. L., Hernándes, Livson, S., Jakobsson, M., Joronen, K. M., Kiviharju, M., et al. (2018) · BMJ · doi:10.1136/bmj.k499 · Cited by 405 · see citing works
Human papillomavirus in cervical cancer and oropharyngeal cancer: One cause, two diseases
Berman, T. A., & Schiller, J. T. (2017) · Cancer · doi:10.1002/cncr.30588 · Cited by 402 · see citing works
Towards a deeper understanding of the vaginal microbiota
France, M., Alizadeh, M. A., Brown, S. E., Ma, B., & Ravel, J. (2022) · Nature Microbiology · doi:10.1038/s41564-022-01083-2 · Cited by 398 · see citing works
Norenhag, J., Du, J., Olovsson, M., Verstraelen, H., Engstrand, L. G., & Brusselaers, N. (2019) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.15854 · Cited by 385 · see citing works
The pathobiome in animal and plant diseases.
Bass, D., Stentiford, G. D., Wang, H.-C., Koskella, B., & Tyler, C. R. (2019) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2019.07.012 · Cited by 376 · see citing works
Brusselaers, N., Shrestha, S., van de Wijgert, J. H. H. M., & Verstraelen, H. (2018) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2018.12.011 · Cited by 321 · see citing works
Cervicovaginal microbiome and natural history of HPV in a longitudinal study
Usyk, M., Zolnik, C. P., Castle, P. E., Porras, C., Herrero, R., Gradíssimo, A., González, P., Safaeian, M., Schiffman, M., Burk, R. D., et al. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008376 · Cited by 316 · see citing works
Paola, M. D., Sani, C., Clemente, A. M., Iossa, A., Perissi, E., Castronovo, G., Tanturli, M., Rivero, D., Cozzolino, F., Cavalieri, D., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-09842-6 · Cited by 305 · see citing works
Ilhan, Z. E., Łaniewski, P., Thomas, N., Roe, D. J., Chase, D. M., & Herbst‐Kralovetz, M. M. (2019) · EBioMedicine · doi:10.1016/j.ebiom.2019.04.028 · Cited by 302 · see citing works
Dzutsev, A., Badger, J. H., Perez-Chanona, E., Roy, S., Salcedo, R., Smith, C. K., & Trinchieri, G. (2017) · Annual Review of Immunology · doi:10.1146/annurev-immunol-051116-052133 · Cited by 302 · see citing works
Łaniewski, P., Barnes, D., Goulder, A., Cui, H., Roe, D. J., Chase, D. M., & Herbst‐Kralovetz, M. M. (2018) · Scientific Reports · doi:10.1038/s41598-018-25879-7 · Cited by 285 · see citing works
Does the vaginal microbiota play a role in the development of cervical cancer?
Kyrgiou, M., Mitra, A., & Moscicki, A. (2016) · Translational research · doi:10.1016/j.trsl.2016.07.004 · Cited by 293 · see citing works
Mitra, A., MacIntyre, D. A., Ntritsos, G., Smith, A., Tsilidis, K. K., Marchesi, J. R., Bennett, P. R., Moscicki, A., & Kyrgiou, M. (2020) · Nature Communications · doi:10.1038/s41467-020-15856-y · Cited by 258 · see citing works
Lewis, F. M. T., Bernstein, K. T., & Aral, S. O. (2017) · Obstetrics & Gynecology · doi:10.1097/aog.0000000000001932 · Cited by 248 · see citing works
Hallmarks of cancer—the new testament
Senga, S. S., & Grose, R. P. (2021) · Open Biology · doi:10.1098/rsob.200358 · Cited by 221 · see citing works
The role of the vaginal microbiome in gynaecological cancer
Champer, M., Wong, A., Champer, J., Brito, I., Messer, P. W., Hou, J., & Wright, J. (2017) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.14631 · Cited by 207 · see citing works
Interplay among Vaginal Microbiome, Immune Response and Sexually Transmitted Viral Infections
Torcia, M. G. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20020266 · Cited by 202 · see citing works
Barrientos‐Durán, A., Fuentes, A. P., de Salazar, A., Plaza‐Díaz, J., & García, F. (2020) · Nutrients · doi:10.3390/nu12020419 · Cited by 183 · see citing works
Curty, G., de Carvalho, P. S., & Soares, M. A. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms21010222 · Cited by 183 · see citing works
Chen, Y., Qiu, X., Wang, W., Li, D., Wu, A., Hong, Z., Di, W. J., & Qiu, L. (2020) · BMC Infectious Diseases · doi:10.1186/s12879-020-05324-9 · Cited by 179 · see citing works
Viral Infections, the Microbiome, and Probiotics
Harper, A., Vijayakumar, V., Ouwehand, A. C., ter Haar, J., Obis, D., Espadaler, J., Binda, S., Desiraju, S., & Day, R. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.596166 · Cited by 177 · see citing works
The pregnancy microbiome and preterm birth
Bayar, E., Bennett, P. R., Chan, D., Sykes, L., & MacIntyre, D. A. (2020) · Seminars in Immunopathology · doi:10.1007/s00281-020-00817-w · Cited by 164 · see citing works
Lebeau, A., Bruyère, D., Roncarati, P., Peixoto, P., Hervouet, É., Cobraiville, G., Taminiau, B., Masson, M., Gallego, C., Mazzucchelli, G., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-28724-8 · Cited by 160 · see citing works
Kalliala, I. E. J., Athanasiou, A., Veroniki, A. A., Salanti, G., Efthimiou, O., Raftis, N., Bowden, S. J., Paraskevaidi, M., Aro, K. L. S., Arbyn, M., et al. (2020) · Annals of Oncology · doi:10.1016/j.annonc.2019.11.004 · Cited by 159 · see citing works
Gupta, S., Palmer, C., Bik, E. M., Cárdenas, J. P., Núñez, H., Kraal, L., Bird, S. W., Bowers, J., Smith, A. J., Walton, N. A., et al. (2018) · Frontiers in Public Health · doi:10.3389/fpubh.2018.00077 · Cited by 157 · see citing works
Vaginal microbiome and cervical cancer
Kyrgiou, M., & Moscicki, A. (2022) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2022.03.005 · Cited by 156 · see citing works
Cervical Carcinoma: Oncobiology and Biomarkers
Volkova, L. V., Pashov, P. A. I., & Omelchuk, N. N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212571 · Cited by 149 · see citing works
The role of probiotics in vaginal health
Mei, Z., & Li, D. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.963868 · Cited by 127 · see citing works
Łaniewski, P., & Herbst‐Kralovetz, M. M. (2021) · npj Biofilms and Microbiomes · doi:10.1038/s41522-021-00259-8 · Cited by 125 · see citing works
Lu, W., He, F., Lin, Z., Liu, S., Li, T., Huang, Y., & Hu, Z. (2020) · International Journal of Cancer · doi:10.1002/ijc.33428 · Cited by 120 · see citing works
Lim, Y., Fukuma, N. M., Totsika, M., Kenny, L., Morrison, M., & Punyadeera, C. (2018) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2018.00267 · Cited by 119 · see citing works
So, K. A., Yang, E. J., Kim, N. R., Hong, S. R., Lee, J.-H., Hwang, C.-S., Shim, S.-H., Lee, S. J., & Kim, T. J. (2020) · PLOS ONE · doi:10.1371/journal.pone.0238705 · Cited by 113 · see citing works
Godoy‐Vitorino, F., Romaguera, J., Zhao, C., Vargas-Robles, D., Ortiz-Morales, G., Vazquez-Sanchez, F. E., Sánchez-Vázquez, M. M., de la Garza-Casillas, M., Martínez‐Ferrer, M., White, J. R., et al. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.02533 · Cited by 116 · see citing works
Diversity of Vaginal Microbiome in Pregnancy: Deciphering the Obscurity
Gupta, P., Singh, M. P., & Goyal, K. (2020) · Frontiers in Public Health · doi:10.3389/fpubh.2020.00326 · Cited by 119 · see citing works
The ecology of human microbiota: dynamics and diversity in health and disease
Karkman, A., Lehtimäki, J., & Ruokolainen, L. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13326 · Cited by 116 · see citing works
The Vaginal Microbiome: A Long Urogenital Colonization Throughout Woman Life
Auriemma, R. S., Scairati, R., Vecchio, G. D., Liccardi, A., Verde, N., Pirchio, R., Pivonello, R., Ercolini, D., & Colao, A. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.686167 · Cited by 114 · see citing works
Role of Lactobacillus in cervical cancer
Yang, X., Da, M., Zhang, W., Quan, Q., Zhang, C., & Han, S. (2018) · Cancer Management and Research · doi:10.2147/cmar.s165228 · Cited by 106 · see citing works
Łaniewski, P., Cui, H., Roe, D. J., Barnes, D., Goulder, A., Monk, B. J., Greenspan, D. L., Chase, D. M., & Herbst‐Kralovetz, M. M. (2019) · Scientific Reports · doi:10.1038/s41598-019-43849-5 · Cited by 106 · see citing works
Microbiome and Cervical Cancer
Castanheira, C. P., Sallas, M. L., Nunes, R. A. L., Lorenzi, N. P. C., & Termini, L. (2020) · Pathobiology · doi:10.1159/000511477 · Cited by 110 · see citing works
Interactions between microbiota and cervical epithelial, immune, and mucus barrier
Dong, M., Dong, Y., Bai, J., Li, H., Ma, X., Li, B., Wang, C., Li, H., Qi, W., Wang, Y., et al. (2023) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2023.1124591 · Cited by 109 · see citing works
Wang, H., Ma, Y., Li, R., Chen, X., Wan, L., & Zhao, W. (2019) · The Journal of Infectious Diseases · doi:10.1093/infdis/jiz325 · Cited by 104 · see citing works
Ntuli, L., Mtshali, A., Mzobe, G. F., Liebenberg, L. J. P., & Ngcapu, S. (2022) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2022.927131 · Cited by 106 · see citing works
Cervical cancer and vaginal microbiota changes
Kovachev, S. M. (2019) · Archives of Microbiology · doi:10.1007/s00203-019-01747-4 · Cited by 97 · see citing works
Vaginal Microbiome in Preterm Rupture of Membranes
Bennett, P. R., Brown, R. G., & MacIntyre, D. A. (2020) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/j.ogc.2020.08.001 · Cited by 95 · see citing works
Tocchetti, C. G., Ameri, P., de Boer, R. A., D’Alessandra, Y., Russo, M., Sorriento, D., Ciccarelli, M., Kiss, B., Bertrand, L., Dawson, D. K., et al. (2020) · Cardiovascular Research · doi:10.1093/cvr/cvaa222 · Cited by 90 · see citing works
Chen, Y., Hong, Z., Wang, W., Gu, L., Gao, H., Qiu, L., & Di, W. J. (2019) · BMC Infectious Diseases · doi:10.1186/s12879-019-4279-6 · Cited by 89 · see citing works
Wu, S., Ding, X., Kong, Y., Acharya, S., Wu, H., Huang, C., Liang, Y., Nong, X., & Chen, H. (2021) · Gynecologic Oncology · doi:10.1016/j.ygyno.2021.08.016 · Cited by 89 · see citing works
The human microbiome and cancer: a diagnostic and therapeutic perspective
Kandalai, S., Li, H., Zhang, N., Peng, H., & Zheng, Q. (2023) · Cancer Biology & Therapy · doi:10.1080/15384047.2023.2240084 · Cited by 93 · see citing works
Moscicki, A., Shi, B., Huang, H., Barnard, E., & Li, H. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.569022 · Cited by 87 · see citing works
Mbulawa, Z. Z. A., van Schalkwyk, C., Hu, N.-C., Meiring, T. L., Barnabas, S. L., Dabee, S., Jaspan, H. B., Kriek, J., Jaumdally, S. Z., Müller, E. E., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0190166 · Cited by 84 · see citing works
HPV infection and bacterial microbiota in the placenta, uterine cervix and oral mucosa
Tuominen, H. K., Rautava, S., Syrjänen, S., Collado, M. C., & Rautava, J. (2018) · Scientific Reports · doi:10.1038/s41598-018-27980-3 · Cited by 80 · see citing works
Bokulich, N. A., Łaniewski, P., Adamov, A., Chase, D. M., Caporaso, J. G., & Herbst‐Kralovetz, M. M. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009876 · Cited by 82 · see citing works
Kesic, V. I., Carcopino, X., Preti, M., Vieira‐Baptista, P., Bevilacqua, F., Bornstein, J., Chargari, C., Cruickshank, M. E., Erzeneoglu, B. E., Gallio, N., et al. (2023) · International Journal of Gynecological Cancer · doi:10.1136/ijgc-2022-004213 · Cited by 79 · see citing works
Vergara, D., Simeone, P., Damato, M., Maffia, M., Lanuti, P., & Trerotola, M. (2019) · Journal of Oncology · doi:10.1155/2019/1253727 · Cited by 77 · see citing works
Depiction of Vaginal Microbiota in Women With High-Risk Human Papillomavirus Infection
Wei, Z., Chen, H., Wang, C., Yang, G., Han, S., & Zhang, S.-L. (2021) · Frontiers in Public Health · doi:10.3389/fpubh.2020.587298 · Cited by 76 · see citing works
Leyva‐Gómez, G., Prado-Audelo, M. L. D., Ortega‐Peña, S., Mendoza‐Muñoz, N., Urbán‐Morlán, Z., González‐Torres, M., Carmen, M. G., Figueroa‐González, G., Reyes‐Hernández, O. D., & Cortés, H. (2019) · Pharmaceutics · doi:10.3390/pharmaceutics11050217 · Cited by 76 · see citing works
Vaginal Microbiota and HPV Infection: Novel Mechanistic Insights and Therapeutic Strategies
Li, Y., Yu, T., Huang, Y., Li, D., Yu, T., Yuan, T., Rahaman, A., Ali, S. M., Farhat, A., Dian, Z., et al. (2020) · Infection and Drug Resistance · doi:10.2147/idr.s210615 · Cited by 75 · see citing works
The interplay between human papillomavirus and vaginal microbiota in cervical cancer development
Sharifian, K., Shoja, Z., & Jalilvand, S. (2023) · Virology Journal · doi:10.1186/s12985-023-02037-8 · Cited by 81 · see citing works
Wiik, J., Sengpiel, V., Kyrgiou, M., Nilsson, S., Mitra, A., Tanbo, T. G., Jonassen, C. M., Tannæs, T. M., & Sjøborg, K. (2019) · BMC Women s Health · doi:10.1186/s12905-019-0727-0 · Cited by 73 · see citing works
Onywera, H., Williamson, A., Mbulawa, Z. Z. A., Coetzee, D. J., & Meiring, T. L. (2019) · Papillomavirus Research · doi:10.1016/j.pvr.2019.04.006 · Cited by 74 · see citing works
From Microbiome to Inflammation: The Key Drivers of Cervical Cancer
Zhou, Z., Long, H., Cheng, Y., Luo, H., Wen, D., & Gao, L. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.767931 · Cited by 76 · see citing works
Zhang, C., Liu, Y., Gao, W., Pan, Y., Gao, Y., Shen, J., & Xiong, H. (2018) · Cancer Medicine · doi:10.1002/cam4.1471 · Cited by 72 · see citing works
Yang, M., Li, L., Jiang, C., Qin, X., Zhou, M., Mao, X., & Xing, H. (2020) · BMC Infectious Diseases · doi:10.1186/s12879-020-05349-0 · Cited by 66 · see citing works
Microbiome factors in HPV-driven carcinogenesis and cancers
Lin, D., Kouzy, R., Jaoude, J. A., Noticewala, S. S., Medrano, A. Y. D., Klopp, A. H., Taniguchi, C. M., & Colbert, L. E. (2020) · PLoS Pathogens · doi:10.1371/journal.ppat.1008524 · Cited by 66 · see citing works
Nicolò, S., Tanturli, M., Mattiuz, G., Antonelli, A., Baccani, I., Bonaiuto, C., Baldi, S., Nannini, G., Menicatti, M., Bartolucci, G., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22126487 · Cited by 65 · see citing works
Association of Cervical Dysbacteriosis, HPV Oncogene Expression, and Cervical Lesion Progression
Liu, H., Liang, H., Li, D., Wang, M., & Li, Y. (2022) · Microbiology Spectrum · doi:10.1128/spectrum.00151-22 · Cited by 65 · see citing works
Comparative analysis of vaginal microbiota sampling using 16S rRNA gene analysis
Virtanen, S., Kalliala, I. E. J., Nieminen, P., & Salonen, A. (2017) · PLoS ONE · doi:10.1371/journal.pone.0181477 · Cited by 65 · see citing works
Mitra, A., MacIntyre, D. A., Paraskevaidi, M., Moscicki, A., Mahajan, V., Smith, A., Lee, Y. S., Lyons, D., Paraskevaidis, E. A., Marchesi, J. R., et al. (2021) · Genome Medicine · doi:10.1186/s13073-021-00977-w · Cited by 64 · see citing works
Huang, X., Li, C., Li, F., Zhao, J., Wan, X., & Wang, K. (2018) · International Journal of Cancer · doi:10.1002/ijc.31342 · Cited by 66 · see citing works
Tango, C. N., Seo, S., Kwon, M., Lee, D.-O., Chang, H. K., & Kim, M. K. (2020) · Scientific Reports · doi:10.1038/s41598-020-66607-4 · Cited by 64 · see citing works
Sneathia: an emerging pathogen in female reproductive disease and adverse perinatal outcomes
Theis, K. R., Сергеевна, Ф. В., Romero, R. J., Borisov, A. B., Winters, A. D., Galaz, J., & Gomez‐Lopez, N. (2021) · Critical Reviews in Microbiology · doi:10.1080/1040841x.2021.1905606 · Cited by 62 · see citing works
Kúdela, E., Líšková, A., Samec, M., Koklesová, L., Holubeková, V., Rokos, T., Kozubík, E., Pribulová, T., Zhai, K., Büsselberg, D., et al. (2021) · The EPMA Journal · doi:10.1007/s13167-021-00244-3 · Cited by 61 · see citing works
Microbes in gynecologic cancers: Causes or consequences and therapeutic potential
Wahid, M., Dar, S. A., Jawed, A., Mandal, R. K., Akhter, N., Khan, S. A., Khan, F., Jogaiah, S., Kumar, A., & Rattan, R. (2021) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2021.07.013 · Cited by 66 · see citing works
Gardella, B., Pasquali, M. F., Verde, M. L., Cianci, S., Torella, M., & Dominoni, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23137174 · Cited by 66 · see citing works
Li, H., Zang, Y., Wang, C., Li, H., Fan, A., Han, C., & Xue, F. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.609488 · Cited by 61 · see citing works
Frąszczak, K., Barczyński, B., & Kondracka, A. (2022) · Cancers · doi:10.3390/cancers14194909 · Cited by 59 · see citing works
Siqueira, J. D., Curty, G., Deng, X., Hofer, C. B., Machado, E. S., Seuánez, H. N., Soares, M. A., Delwart, E., & Soares, E. A. J. M. (2019) · Viruses · doi:10.3390/v11050422 · Cited by 57 · see citing works
Kang, G.-U., Jung, D.-R., Lee, Y. H., Jeon, S. Y., Han, H. S., Chong, G. O., & Shin, J. (2021) · Microorganisms · doi:10.3390/microorganisms9020294 · Cited by 60 · see citing works
Usyk, M., Schlecht, N. F., Pickering, S., Williams, L., Sollecito, C. C., Gradíssimo, A., Porras, C., Safaeian, M., Pinto, L. A., Herrero, R., et al. (2022) · Nature Communications · doi:10.1038/s41467-021-27628-3 · Cited by 57 · see citing works
Ritu, W., Enqi, W., Zheng, S., Wang, J., Ling, Y., & Wang, Y. (2018) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-18-0233 · Cited by 57 · see citing works
The Microbiome and Gynecologic Cancer: Current Evidence and Future Opportunities
Chambers, L., Bussies, P. L., Vargas, R., Esakov, E. L., Tewari, S., Reizes, O., & Michener, C. M. (2021) · Current Oncology Reports · doi:10.1007/s11912-021-01079-x · Cited by 59 · see citing works
Curty, G., Costa, R. L., Siqueira, J. D., Meyrelles, Â. R., Machado, E. S., Soares, E. A. J. M., & Soares, M. A. (2017) · Scientific Reports · doi:10.1038/s41598-017-17351-9 · Cited by 54 · see citing works
Cascardi, E., Cazzato, G., Daniele, A., Silvestris, E., Cormio, G., Vagno, G. D., Malvası, A., Loizzi, V., Scacco, S., Pinto, V., et al. (2022) · Biology · doi:10.3390/biology11081114 · Cited by 55 · see citing works
Zhang, H., Lu, J., Lü, Y., Cai, Q., Liu, H., & Xu, C. (2018) · Scientific Reports · doi:10.1038/s41598-018-23389-0 · Cited by 53 · see citing works
Role of Microbiota in Viral Infections and Pathological Progression
Mizutani, T., Ishizaka, A., Koga, M., Tsutsumi, T., & Yotsuyanagi, H. (2022) · Viruses · doi:10.3390/v14050950 · Cited by 50 · see citing works
Kwon, M., Seo, S., Kim, M. K., Lee, D. O., & Lim, M. C. (2019) · Cancers · doi:10.3390/cancers11030309 · Cited by 50 · see citing works
How the Cervical Microbiota Contributes to Cervical Cancer Risk in Sub-Saharan Africa
Klein, C., Kahesa, C., Mwaiselage, J. D., West, J. T., Wood, C. A., & Angeletti, P. C. (2020) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2020.00023 · Cited by 49 · see citing works
Kaelin, E. A., Skidmore, P. T., Łaniewski, P., Holland, L. A., Chase, D. M., Herbst‐Kralovetz, M. M., & Lim, E. S. (2022) · mSystems · doi:10.1128/msystems.00064-22 · Cited by 47 · see citing works
Aerobic Vaginitis—Underestimated Risk Factor for Cervical Intraepithelial Neoplasia
Plisko, O., Žodžika, J., Jermakova, I., Pčolkina, K., Prusakevica, A., Liepniece‐Karele, I., Donders, G. G. G., & Rezeberga, D. (2021) · Diagnostics · doi:10.3390/diagnostics11010097 · Cited by 46 · see citing works
Molecular aspects of cervical cancer: a pathogenesis update
Vallejo‐Ruiz, V., Gutiérrez‐Xicoténcatl, L., Contreras, O. M., & Lizano, M. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1356581 · Cited by 45 · see citing works
Host-Microbiome Interaction and Cancer: Potential Application in Precision Medicine
Contreras, A. V., Cocom-Chan, B., Hernández‐Montes, G., Portillo-Bobadilla, T., & Reséndis-Antonio, O. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00606 · Cited by 46 · see citing works
Organ‐on‐a‐Chip Systems for Women's Health Applications
Nawroth, J. C., Rogal, J., Weiß, M., Brucker, S. Y., & Loskill, P. (2017) · Advanced Healthcare Materials · doi:10.1002/adhm.201700550 · Cited by 44 · see citing works
Serrano, L., López, A. C., Rodríguez, S. P. G., Palacios, S., Dexeus, D., Centeno, C., Coronado, P., de la Fuente, J., López, J. A., Vanrell, C., et al. (2021) · Journal of Lower Genital Tract Disease · doi:10.1097/lgt.0000000000000596 · Cited by 44 · see citing works
Ventolini, G., Vieira‐Baptista, P., Seta, F. D., Verstraelen, H., Hoffmann, R., & Lev‐Sagie, A. (2021) · Journal of Lower Genital Tract Disease · doi:10.1097/lgt.0000000000000646 · Cited by 42 · see citing works
- Authors
- Mitra, A., MacIntyre, D. A., Lee, Y. S., Smith, A., Marchesi, J. R., Lehne, B., Bhatia, R., Lyons, D., Paraskevaidis, E., Li, J. V., Holmes, E., Nicholson, J. K., Bennett, P. R., & Kyrgiou, M.
- Affiliations
- Hammersmith Hospital (GB)
- Imperial College London (GB)
- Cardiff University (GB)
- University of Edinburgh (GB)
- Imperial College Healthcare NHS Trust (GB)
- University Hospital of Ioannina (GR)
- Corresponding author
- Kyrgiou, M.
- ORCID
- Venue
- Scientific Reports
- Published
- 2015-11-17
- Volume
- 5
- Issue
- 1
- Pages
- 16865-16865
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC4648063
- OpenAlex
- W2201127965
- Cited by
- 498
- References
- 46
- Citations by year
- 2026: 42 · 2025: 54 · 2024: 54 · 2023: 60 · 2022: 64 · 2021: 82 · 2020: 48 · 2019: 32 · 2018: 26 · 2017: 22 · 2016: 13
- FWCI
- 16.94
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- ORCA Online Research @Cardiff (Cardiff University) (acceptedVersion)
- UWE Research Repository (UWE Bristol) (submittedVersion, cc-by)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
- Funders
- Genesis Research Trust
- Imperial College Healthcare Charity
- National Institute for Health and Care Research (ACF-2014-21-012, P45272)
- Imperial College London (P45272)
- Imperial College Healthcare NHS Trust (P45272)
- Medical Research Council (MR/L009226/1)
- Topics
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Health Sciences › Medicine › Epidemiology › Cervical Cancer and HPV Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- cervical intraepithelial neoplasia, vaginal microbiota, microbiome diversity, disease progression, human papillomavirus, persistent HPV infection, Lactobacillus, low-grade squamous intraepithelial lesion, high-grade squamous intraepithelial lesion, invasive cervical cancer, Sneathia sanguinegens, Anaerococcus tetradius, Peptostreptococcus anaerobius, Lactobacillus jensenii
- MeSH terms
- Adult, Uterine Cervical Dysplasia, Uterine Cervical Neoplasms, DNA, Viral, Female, Genotype, Humans, Lactobacillus, Middle Aged, Peptostreptococcus, RNA, Ribosomal, 16S, Severity of Illness Index, Vagina, Cohort Studies, Biomarkers, Disease Progression, Papillomaviridae, Biodiversity, Young Adult, Microbiota
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