{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,21]],"date-time":"2026-10-21T04:34:02Z","timestamp":1792557242993,"version":"4.5.0"},"reference-count":35,"publisher":"Akademiai Kiado Zrt.","issue":"3","content-domain":{"domain":["akjournals.com"],"crossmark-restriction":true},"short-container-title":["AMicr"],"published-print":{"date-parts":[[2024,9,18]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Although the relationship between vaginal microorganisms and fertility has been well established, only few studies have investigated vaginal microorganisms in women undergoing <jats:italic>in vitro<\/jats:italic> fertilization (IVF). Our aim was to study the differences in vaginal microbiota between infertile women with repeated implantation failure (RIF) and those who achieved clinical pregnancy in their first frozen embryo transfer cycle. We compared the vaginal microbiota of patients with a history of RIF (<jats:italic>n<\/jats:italic> = 37) with that of the control group (<jats:italic>n<\/jats:italic> = 43). Following DNA extraction, metagenomic sequencing was employed for the analysis of alpha and beta diversities, distinctions in bacterial species, and the functional annotation of microbial genes. Furthermore, disparities between the two groups were revealed. Alpha diversity analysis revealed that the Shannon index was higher in the RIF group (<jats:italic>P<\/jats:italic> &lt; 0.05). There were differences in the beta diversity between groups (<jats:italic>P<\/jats:italic> = 0.16). At the bacterial family level, the relative abundance of Actinomycetaceae (<jats:italic>P<\/jats:italic> = 0.013) and Ruminococcaceae (<jats:italic>P<\/jats:italic> = 0.013) were significantly higher in the RIF group. At the genus level, the abundances of Actinomyces (<jats:italic>P<\/jats:italic> = 0.028) and Subdoligranulum (<jats:italic>P<\/jats:italic> = 0.013) were\u00a0significantly higher in the RIF group. At the species level, the abundances of <jats:italic>Prevotella timonensis<\/jats:italic> (<jats:italic>P<\/jats:italic> = 0.028), <jats:italic>Lactobacillus jensenii<\/jats:italic> (<jats:italic>P<\/jats:italic> = 0.049), and Subdoligranulum (<jats:italic>P<\/jats:italic> = 0.013) were significantly higher in the RIF group. Significant differences in family, genus, species, alpha and beta diversity were observed in the vaginal microbiota between groups. Notably, among these findings, the Subdoligranulum genus emerged as the most prominent correlating factor.<\/jats:p>","DOI":"10.1556\/030.2024.02323","type":"journal-article","created":{"date-parts":[[2024,8,23]],"date-time":"2024-08-23T11:16:02Z","timestamp":1724411762000},"page":"263-271","update-policy":"https:\/\/doi.org\/10.1556\/policypage.crossmark.crossref.2","source":"Crossref","is-referenced-by-count":4,"title":["Characterization of the vaginal microbiota in\u00a0infertile women with repeated implantation failure"],"prefix":"10.1556","volume":"71","author":[{"given":"Lidan","family":"Liu","sequence":"first","affiliation":[{"name":"Guangxi Reproductive Medicine Center, The First Affiliated Hospital of Guangxi Medical University, Nanning, Guangxi, 530021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tong","family":"Feng","sequence":"additional","affiliation":[{"name":"State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources, Guangxi University, Nanning, Guangxi, 530000, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingyou","family":"Liu","sequence":"additional","affiliation":[{"name":"Guangdong Provincial Key Laboratory of Animal Molecular Design and Precise Breeding, School of Life Science and Engineering, Foshan University, Foshan, Guangdong, 528225, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ming","family":"Liao","sequence":"additional","affiliation":[{"name":"Guangxi Reproductive Medicine Center, The First Affiliated Hospital of Guangxi Medical University, Nanning, Guangxi, 530021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo","family":"Liu","sequence":"additional","affiliation":[{"name":"Guangxi Reproductive Medicine Center, The First Affiliated Hospital of Guangxi Medical University, Nanning, Guangxi, 530021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0004-8862-1430","authenticated-orcid":true,"given":"Mujun","family":"Li","sequence":"additional","affiliation":[{"name":"Guangxi Reproductive Medicine Center, The First Affiliated Hospital of Guangxi Medical University, Nanning, Guangxi, 530021, China"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"425","reference":[{"key":"B1","series-title":"Clin Biochem","first-page":"2","article-title":"Fertility and infertility: definition and epidemiology","volume":"62","author":"Borght MV","year":"2018","unstructured":"Borght MV, Wyns C. Fertility and infertility: definition and epidemiology. Clin Biochem 2018; 62: 2\u201310."},{"issue":"3","key":"B2","series-title":"J Assist Reprod Genet","first-page":"433","article-title":"Cumulus-corona gene expression analysis combined with morphological embryo scoring in single embryo transfer cycles increases live birth after fresh transfer and decreases time to pregnancy","volume":"36","author":"Adriaenssens T","year":"2019","unstructured":"Adriaenssens T, Van Vaerenbergh I, Coucke W, Segers I, Verheyen G, Anckaert E, et\u00a0al. Cumulus-corona gene expression analysis combined with morphological embryo scoring in single embryo transfer cycles increases live birth after fresh transfer and decreases time to pregnancy. J Assist Reprod Genet 2019; 36(3): 433\u2013443."},{"issue":"1","key":"B3","series-title":"Reprod Biomed Online","first-page":"14","article-title":"Recurrent implantation failure: definition and management","volume":"28","author":"Coughlan C","year":"2014","unstructured":"Coughlan C, Ledger W, Wang Q, Liu F, Demirol A, Gurgan T, et\u00a0al. Recurrent implantation failure: definition and management. Reprod Biomed Online 2014; 28(1): 14\u201338."},{"issue":"3","key":"B4","series-title":"mBio","first-page":"e03242","article-title":"Alterations in vaginal microbiota and associated metabolome in women with recurrent implantation failure","volume":"11","author":"Fu M","year":"2020","unstructured":"Fu M, Zhang X, Liang Y, Lin S, Qian W, Fan S. Alterations in vaginal microbiota and associated metabolome in women with recurrent implantation failure. mBio 2020; 11(3): e03242\u201319."},{"issue":"14","key":"B5","series-title":"J\u00a0Biol Chem","first-page":"5230","article-title":"Identification and characterization of NanH2 and NanH3, enzymes responsible for sialidase activity in the vaginal bacterium Gardnerella vaginalis","volume":"294","author":"Robinson LS","year":"2019","unstructured":"Robinson LS, Schwebke J, Lewis WG, Lewis AL. Identification and characterization of NanH2 and NanH3, enzymes responsible for sialidase activity in the vaginal bacterium Gardnerella vaginalis. J\u00a0Biol Chem 2019; 294(14): 5230\u20135245."},{"issue":"5","key":"B6","series-title":"J Urol","first-page":"2050","article-title":"Adherence of Lactobacillus crispatus to vaginal epithelial cells from women with or without a history of recurrent urinary tract infection","volume":"176","author":"Kwok L","year":"2006","unstructured":"Kwok L, Stapleton AE, Stamm WE, Hillier SL, Wobbe CL, Gupta K. Adherence of Lactobacillus crispatus to vaginal epithelial cells from women with or without a history of recurrent urinary tract infection. J Urol 2006; 176(5): 2050\u20134, discussion 2054."},{"issue":"12","key":"B7","series-title":"Matern Child Health J","first-page":"2682","article-title":"First trimester levels of BV-associated bacteria and risk of miscarriage among women early in pregnancy","volume":"19","author":"Nelson DB","year":"2015","unstructured":"Nelson DB, Hanlon AL, Wu G, Liu C, Fredricks DN. First trimester levels of BV-associated bacteria and risk of miscarriage among women early in pregnancy. Matern Child Health J 2015; 19(12): 2682\u20137."},{"issue":"2","key":"B8","series-title":"Paediatr Perinat Epidemiol","first-page":"88","article-title":"Early pregnancy changes in bacterial vaginosis-associated bacteria and preterm delivery","volume":"28","author":"Nelson DB","year":"2014","unstructured":"Nelson DB, Hanlon A, Nachamkin I, Haggerty C, Mastrogiannis DS, Liu C, et\u00a0al. Early pregnancy changes in bacterial vaginosis-associated bacteria and preterm delivery. Paediatr Perinat Epidemiol 2014; 28(2): 88\u201396."},{"issue":"2","key":"B9","series-title":"BJOG","first-page":"200","article-title":"Reproductive outcome of patients undergoing in vitro fertilisation treatment and diagnosed with bacterial vaginosis or abnormal vaginal microbiota: a systematic PRISMA review and meta-analysis","volume":"126","author":"Haahr T","year":"2019","unstructured":"Haahr T, Zacho J, Br\u00e4uner M, Shathmigha K, Skov Jensen J, Humaidan P. Reproductive outcome of patients undergoing in vitro fertilisation treatment and diagnosed with bacterial vaginosis or abnormal vaginal microbiota: a systematic PRISMA review and meta-analysis. BJOG 2019; 126(2): 200\u2013207."},{"issue":"5","key":"B10","series-title":"Am J Reprod Immunol","article-title":"Investigating the effect of an abnormal cervico-vaginal and endometrial microbiome on assisted reproductive technologies: a systematic review","volume":"80","author":"Bracewell-Milnes T","year":"2018","unstructured":"Bracewell-Milnes T, Saso S, Nikolaou D, Norman-Taylor J, Johnson M, Thum MY. Investigating the effect of an abnormal cervico-vaginal and endometrial microbiome on assisted reproductive technologies: a systematic review. Am J Reprod Immunol 2018; 80(5): e13037."},{"key":"B11","article-title":"Preembryo Grading. Atlas of the Human Oocyte and Early Conceptus","author":"Veeck LL","year":"1991","unstructured":"Veeck LL. Preembryo Grading. Atlas of the Human Oocyte and Early Conceptus; 1991."},{"issue":"18","key":"B12","series-title":"Ann Transl Med","first-page":"1161","article-title":"Association of high-risk human papillomavirus infection duration and cervical lesions with vaginal microbiota composition","volume":"8","author":"Liu J","year":"2020","unstructured":"Liu J, Luo M, Zhang Y, Cao G, Wang S. Association of high-risk human papillomavirus infection duration and cervical lesions with vaginal microbiota composition. Ann Transl Med 2020; 8(18): 1161."},{"issue":"15","key":"B13","series-title":"Bioinformatics","first-page":"2114","article-title":"Trimmomatic: a flexible trimmer for Illumina sequence data","volume":"30","author":"Bolger AM","year":"2014","unstructured":"Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 2014; 30(15): 2114\u201320."},{"issue":"4","key":"B14","series-title":"Nat Biotechnol","first-page":"422","article-title":"Efficient hybrid de novo assembly of human genomes with WENGAN","volume":"39","author":"Di Genova A","year":"2021","unstructured":"Di Genova A, Buena-Atienza E, Ossowski S, Sagot MF. Efficient hybrid de novo assembly of human genomes with WENGAN. Nat Biotechnol 2021; 39(4): 422\u2013430."},{"issue":"4","key":"B15","series-title":"Nat Methods","first-page":"357","article-title":"Fast gapped-read alignment with Bowtie 2","volume":"9","author":"Langmead B","year":"2012","unstructured":"Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9(4): 357\u20139."},{"issue":"10","key":"B16","series-title":"Nat Methods","first-page":"902","article-title":"MetaPhlAn2 for enhanced metagenomic taxonomic profiling","volume":"12","author":"Truong DT","year":"2015","unstructured":"Truong DT, Franzosa EA, Tickle TL, Scholz M, Weingart G, Pasolli E, et\u00a0al. MetaPhlAn2 for enhanced metagenomic taxonomic profiling. Nat Methods 2015; 12(10): 902\u20133."},{"issue":"1","key":"B17","series-title":"Nat Commun","first-page":"1106","article-title":"Expanded catalog of microbial genes and metagenome-assembled genomes from the pig gut microbiome","volume":"12","author":"Chen C","year":"2021","unstructured":"Chen C, Zhou Y, Fu H, Xiong X, Fang S, Jiang H, et\u00a0al. Expanded catalog of microbial genes and metagenome-assembled genomes from the pig gut microbiome. 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Microbiome 2021; 9(1): 68."},{"issue":"5","key":"B20","series-title":"Genome Res","first-page":"824","article-title":"metaSPAdes: a new versatile metagenomic assembler","volume":"27","author":"Nurk S","year":"2017","unstructured":"Nurk S, Meleshko D, Korobeynikov A, Pevzner PA. metaSPAdes: a new versatile metagenomic assembler. Genome Res 2017; 27(5): 824\u2013834."},{"key":"B21","series-title":"Methods","first-page":"3","article-title":"MEGAHIT v1. 0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices","volume":"102","author":"Li D","year":"2016","unstructured":"Li D, Luo R, Liu CM, Leung CM, Ting HF, Sadakane K, et\u00a0al. MEGAHIT v1. 0: a fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods 2016; 102: 3\u201311."},{"issue":"12","key":"B22","series-title":"Nucleic Acids Res","article-title":"Ab initio gene identification in metagenomic sequences","volume":"38","author":"Zhu W","year":"2010","unstructured":"Zhu W, Lomsadze A, Borodovsky M. Ab initio gene identification in metagenomic sequences. Nucleic Acids Res 2010; 38(12): e132."},{"issue":"14","key":"B23","series-title":"Bioinformatics","first-page":"2068","article-title":"Prokka: rapid prokaryotic genome annotation","volume":"30","author":"Seemann T.","year":"2014","unstructured":"Seemann T. Prokka: rapid prokaryotic genome annotation. 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Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol Biol Evol 2017; 34(8): 2115\u20132122."},{"issue":"12","key":"B26","series-title":"Genome Biol","first-page":"550","article-title":"Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2","volume":"15","author":"Love MI","year":"2014","unstructured":"Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 2014; 15(12): 550."},{"issue":"9","key":"B27","first-page":"1","article-title":"Package \u2018vegan\u2019. Community ecology package, version","volume":"2","author":"Oksanen J","year":"2013","unstructured":"Oksanen J, Simpson GL, Blanchet FG, Kindt R, Legendre P, Minchin PR, et al. Package \u2018vegan\u2019. Community ecology package, version. 2013; 2(9): 1-295."},{"issue":"10","key":"B28","series-title":"J Assist Reprod Genet","first-page":"2111","article-title":"Effect of the vaginal microbiome on the pregnancy rate in women receiving assisted reproductive treatment","volume":"36","author":"Bernabeu A","year":"2019","unstructured":"Bernabeu A, Lledo B, D\u00edaz MC, Lozano FM, Ruiz V, Fuentes A, et\u00a0al. Effect of the vaginal microbiome on the pregnancy rate in women receiving assisted reproductive treatment. J Assist Reprod Genet 2019; 36(10): 2111\u20132119."},{"issue":"1","key":"B29","series-title":"Clin Endocrinol(Oxf)","first-page":"52","article-title":"Association between polycystic ovary syndrome and the vaginal microbiome: a case-control study","volume":"93","author":"Hong X","year":"2020","unstructured":"Hong X, Qin P, Huang K, Ding X, Ma J, Xuan Y, et\u00a0al. Association between polycystic ovary syndrome and the vaginal microbiome: a case-control study. 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Gynecol Obstet Invest 2005; 59(3): 175\u20138."},{"issue":"6","key":"B35","series-title":"Hum Reprod","first-page":"1042","article-title":"The vaginal microbiome as a predictor for outcome of in vitro fertilization with or without intracytoplasmic sperm injection: a prospective study","volume":"34","author":"Koedooder R","year":"2019","unstructured":"Koedooder R, Singer M, Schoenmakers S, Savelkoul PHM, Morr\u00e9 SA, de Jonge JD, et\u00a0al. The vaginal microbiome as a predictor for outcome of in vitro fertilization with or without intracytoplasmic sperm injection: a prospective study. 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