Intrauterine colonization with Gardnerella vaginalis and Mobiluncus mulieris induces maternal inflammation but not preterm birth in a mouse model.
intrauterine infection
intrauterine inflammation
mouse model
preterm birth
vaginal microbiome
Journal
American journal of reproductive immunology (New York, N.Y. : 1989)
ISSN: 1600-0897
Titre abrégé: Am J Reprod Immunol
Pays: Denmark
ID NLM: 8912860
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
revised:
28
06
2023
received:
04
04
2023
accepted:
29
06
2023
medline:
27
7
2023
pubmed:
26
7
2023
entrez:
26
7
2023
Statut:
ppublish
Résumé
Preterm birth (PTB) remains a leading cause of childhood mortality. Recent studies demonstrate that the risk of spontaneous PTB (sPTB) is increased in individuals with Lactobacillus-deficient vaginal microbial communities. One proposed mechanism is that vaginal microbes ascend through the cervix, colonize the uterus, and activate inflammatory pathways leading to sPTB. This study assessed whether intrauterine colonization with either Gardnerella vaginalis and Mobiluncus mulieris alone is sufficient to induce maternal-fetal inflammation and induce sPTB. C56/B6J mice, on embryonic day 15, received intrauterine inoculation of saline or 10 Six hours following intrauterine inoculation with G. vaginalis, M. mulieris, or L. crispatus, live bacteria were observed in both blood and amniotic fluid, and a potent immune response was identified in the uterus and maternal serum. In contrast, only a limited immune response was identified in the amniotic fluid and the fetus after intrauterine inoculation. High bacterial load (10 Despite inducing an immune response, intrauterine infusion of live G. vaginalis or M. mulieris is not sufficient to induce sPTB in our mouse model. These results suggest that ascension of common vaginal microbes into the uterine cavity alone is not causative for sPTB.
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13749Subventions
Organisme : NIH HHS
ID : R01 HD098867
Pays : United States
Organisme : NIH HHS
ID : R01 HD102318
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA016520
Pays : United States
Informations de copyright
© 2023 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Blencowe H, Cousens S, Oestergaard MZ, et al. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet. 2012;379(9832):2162-2172. doi:10.1016/S0140-6736(12)60820-4. PubMed PMID: 22682464.
Liu L, Johnson HL, Cousens S, et al. Child Health Epidemiology Reference Group of WHO, Unicef. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000. Lancet. 2012;379(9832):2151-2161. doi:10.1016/S0140-6736(12)60560-1. Epub 20120511. PubMed PMID: 22579125.
Blencowe H, Lee AC, Cousens S, et al. Preterm birth-associated neurodevelopmental impairment estimates at regional and global levels for 2010. Pediatr Res. 2013;74(1):17-34. doi:10.1038/pr.2013.204. Suppl. PubMed PMID: 24366461; PMCID: PMC3873710.
Bhutta AT, Cleves MA, Casey PH, Cradock MM, Anand KJ. Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA. 2002;288(6):728-737. doi:10.1001/jama.288.6.728. PubMed PMID: 12169077.
Boyle AK, Rinaldi SF, Norman JE, Stock SJ. Preterm birth: inflammation, fetal injury and treatment strategies. J Reprod Immunol. 2017;119:62-66. doi:10.1016/j.jri.2016.11.008. Epub 20161202. PubMed PMID: 28122664.
Goldenberg RL, Culhane JF, Iams JD, Romero R. Epidemiology and causes of preterm birth. Lancet. 2008;371(9606):75-84. doi:10.1016/S0140-6736(08)60074-4. PubMed PMID: 18177778; PMCID: PMC7134569.
Kemp MW. Preterm birth, intrauterine infection, and fetal inflammation. Front Immunol. 2014;5:574. doi:10.3389/fimmu.2014.00574. Epub 20141201. PubMed PMID: 25520716; PMCID: PMC4249583.
Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med. 2000;342(20):1500-1507. doi:10.1056/NEJM200005183422007. PubMed PMID: 10816189.
Goncalves LF, Chaiworapongsa T, Romero R. Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev. 2002;8(1):3-13. doi:10.1002/mrdd.10008. PubMed PMID: 11921380.
Romero R, Salafia CM, Athanassiadis AP, et al. The relationship between acute inflammatory lesions of the preterm placenta and amniotic fluid microbiology. Am J Obstet Gynecol. 1992;166(5):1382-1388. doi:10.1016/0002-9378(92)91609-e. PubMed PMID: 1595794.
Russell P. Inflammatory lesions of the human placenta. III. The histopathology of villitis of unknown aetiology. Placenta. 1980;1(3):227-244. doi:10.1016/s0143-4004(80)80005-1. PubMed PMID: 7443642.
Mueller-Heubach E, Rubinstein DN, Schwarz SS. Histologic chorioamnionitis and preterm delivery in different patient populations. Obstet Gynecol. 1990;75(4):622-626. PubMed PMID: 2314782.
Yoon BH, Romero R, Park JS, et al. The relationship among inflammatory lesions of the umbilical cord (funisitis), umbilical cord plasma interleukin 6 concentration, amniotic fluid infection, and neonatal sepsis. Am J Obstet Gynecol. 2000;183(5):1124-1129. doi:10.1067/mob.2000.109035. PubMed PMID: 11084553.
Ustun C, Kocak I, Baris S, Uzel A, Saltik F. Subclinical chorioamnionitis as an etiologic factor in preterm deliveries. Int J Gynaecol Obstet. 2001;72(2):109-115. doi:10.1016/s0020-7292(00)00280-0. PubMed PMID: 11166743.
Ravel J, Gajer P, Abdo Z, et al. Vaginal microbiome of reproductive-age women. Proc Natl Acad Sci U S A. 2011;108(1):4680-4687. doi:10.1073/pnas.1002611107. Suppl. Epub 20100603. PubMed PMID: 20534435; PMCID: PMC3063603.
France M, Alizadeh M, Brown S, Ma B, Ravel J. Towards a deeper understanding of the vaginal microbiota. Nat Microbiol. 2022;7(3):367-378. doi:10.1038/s41564-022-01083-2. Epub 20220304. PubMed PMID: 35246662; PMCID: PMC8910585.
Haahr T, Jensen JS, Thomsen L, Duus L, Rygaard K, Humaidan P. Abnormal vaginal microbiota may be associated with poor reproductive outcomes: a prospective study in IVF patients. Hum Reprod. 2016;31(4):795-803. doi:10.1093/humrep/dew026. Epub 20160223. PubMed PMID: 26911864.
Ravel J, Moreno I, Simon C. Bacterial vaginosis and its association with infertility, endometritis, and pelvic inflammatory disease. Am J Obstet Gynecol. 2021;224(3):251-257. doi:10.1016/j.ajog.2020.10.019. Epub 20201019.. PubMed PMID: 33091407.
Chan D, Bennett PR, Lee YS, et al. Microbial-driven preterm labour involves crosstalk between the innate and adaptive immune response. Nat Commun. 2022;13(1):975. doi:10.1038/s41467-022-28620-1. Epub 20220221. PubMed PMID: 35190561; PMCID: PMC8861006.
Kenyon C, Colebunders R, Crucitti T. The global epidemiology of bacterial vaginosis: a systematic review. Am J Obstet Gynecol. 2013;209(6):505-523. doi:10.1016/j.ajog.2013.05.006. Epub 20130506. PubMed PMID: 23659989.
Force USPST, Owens DK, Davidson KW, et al. Screening for bacterial vaginosis in pregnant persons to prevent preterm delivery: US preventive services task force recommendation statement. JAMA. 2020;323(13):1286-1292. doi:10.1001/jama.2020.2684. PubMed PMID: 32259236.
Leitich H, Kiss H. Asymptomatic bacterial vaginosis and intermediate flora as risk factors for adverse pregnancy outcome. Best Pract Res Clin Obstet Gynaecol. 2007;21(3):375-390. doi:10.1016/j.bpobgyn.2006.12.005. Epub 20070122. PubMed PMID: 17241817.
Hillier SL, Nugent RP, Eschenbach DA, et al. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. The Vaginal Infections and Prematurity Study Group. N Engl J Med. 1995;333(26):1737-1742. doi:10.1056/NEJM199512283332604. PubMed PMID: 7491137.
Holst E, Goffeng AR, Andersch B. Bacterial vaginosis and vaginal microorganisms in idiopathic premature labor and association with pregnancy outcome. J Clin Microbiol. 1994;32(1):176-186. doi:10.1128/jcm.32.1.176-186.1994. PubMed PMID: 8126176; PMCID: PMC262991.
Hay PE, Lamont RF, Taylor-Robinson D, Morgan DJ, Ison C, Pearson J. Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. BMJ. 1994;308(6924):295-298. doi:10.1136/bmj.308.6924.295. PubMed PMID: 8124116; PMCID: PMC2539287.
Riduan JM, Hillier SL, Utomo B, Wiknjosastro G, Linnan M, Kandun N. Bacterial vaginosis and prematurity in Indonesia: association in early and late pregnancy. Am J Obstet Gynecol. 1993;169(1):175-178. doi:10.1016/0002-9378(93)90157-e. PubMed PMID: 8333449.
Kurki T, Sivonen A, Renkonen OV, Savia E, Ylikorkala O. Bacterial vaginosis in early pregnancy and pregnancy outcome. Obstet Gynecol. 1992;80(2):173-177. PubMed PMID: 1635726.
Martius J, Krohn MA, Hillier SL, Stamm WE, Holmes KK, Eschenbach DA. Relationships of vaginal Lactobacillus species, cervical Chlamydia trachomatis, and bacterial vaginosis to preterm birth. Obstet Gynecol. 1988;71(1):89-95. PubMed PMID: 3336545.
Gravett MG, Nelson HP, DeRouen T, Critchlow C, Eschenbach DA, Holmes KK. Independent associations of bacterial vaginosis and Chlamydia trachomatis infection with adverse pregnancy outcome. JAMA. 1986;256(14):1899-1903. PubMed PMID: 3761496.
Brown RG, Al-Memar M, Marchesi JR, et al. Establishment of vaginal microbiota composition in early pregnancy and its association with subsequent preterm prelabor rupture of the fetal membranes. Transl Res. 2019;207:30-43. doi:10.1016/j.trsl.2018.12.005. Epub 20181227. PubMed PMID: 30633889; PMCID: PMC6489901.
Brown RG, Marchesi JR, Lee YS, et al. Vaginal dysbiosis increases risk of preterm fetal membrane rupture, neonatal sepsis and is exacerbated by erythromycin. BMC Med. 2018;16(1):9. doi:10.1186/s12916-017-0999-x. Epub 20180124. PubMed PMID: 29361936; PMCID: PMC5782380.
Callahan BJ, DiGiulio DB, Goltsman DSA, et al. Replication and refinement of a vaginal microbial signature of preterm birth in two racially distinct cohorts of US women. Proc Natl Acad Sci U S A. 2017;114(37):9966-9971. doi:10.1073/pnas.1705899114. Epub 20170828. PubMed PMID: 28847941; PMCID: PMC5604014.
Elovitz MA, Gajer P, Riis V, et al. Cervicovaginal microbiota and local immune response modulate the risk of spontaneous preterm delivery. Nat Commun. 2019;10(1):1305. doi:10.1038/s41467-019-09285-9. Epub 20190321. PubMed PMID: 30899005; PMCID: PMC6428888.
Feehily C, Crosby D, Walsh CJ, et al. Shotgun sequencing of the vaginal microbiome reveals both a species and functional potential signature of preterm birth. NPJ Biofilms Microbiomes. 2020;6(1):50. doi:10.1038/s41522-020-00162-8. Epub 20201112. PubMed PMID: 33184260; PMCID: PMC7665020.
Freitas AC, Bocking A, Hill JE, Money DM, Group VR. Increased richness and diversity of the vaginal microbiota and spontaneous preterm birth. Microbiome. 2018;6(1):117. doi:10.1186/s40168-018-0502-8. Epub 20180628. PubMed PMID: 29954448; PMCID: PMC6022438.
Kindinger LM, Bennett PR, Lee YS, et al. The interaction between vaginal microbiota, cervical length, and vaginal progesterone treatment for preterm birth risk. Microbiome. 2017;5(1):6. doi:10.1186/s40168-016-0223-9. Epub 20170119. PubMed PMID: 28103952; PMCID: PMC5244550.
Kindinger LM, MacIntyre DA, Lee YS, et al. Relationship between vaginal microbial dysbiosis, inflammation, and pregnancy outcomes in cervical cerclage. Sci Transl Med. 2016;8(350):350ra102. doi:10.1126/scitranslmed.aag1026. PubMed PMID: 27488896.
Nelson DB, Hanlon A, Nachamkin I, et al. Early pregnancy changes in bacterial vaginosis-associated bacteria and preterm delivery. Paediatr Perinat Epidemiol. 2014;28(2):88-96. doi:10.1111/ppe.12106. Epub 20140109. PubMed PMID: 24405280; PMCID: PMC4031320.
Romero R, Hassan SS, Gajer P, et al. The vaginal microbiota of pregnant women who subsequently have spontaneous preterm labor and delivery and those with a normal delivery at term. Microbiome. 2014;2:18. doi:10.1186/2049-2618-2-18. Epub 20140527. PubMed PMID: 24987521; PMCID: PMC4066267.
Stafford GP, Parker JL, Amabebe E, et al. Spontaneous preterm birth is associated with differential expression of vaginal metabolites by lactobacilli-dominated microflora. Front Physiol. 2017;8:615. doi:10.3389/fphys.2017.00615. Epub 20170823. PubMed PMID: 28878691; PMCID: PMC5572350.
Hillier SL, Martius J, Krohn M, Kiviat N, Holmes KK, Eschenbach DA. A case-control study of chorioamnionic infection and histologic chorioamnionitis in prematurity. N Engl J Med. 1988;319(15):972-978. doi:10.1056/NEJM198810133191503. PubMed PMID: 3262199.
Gravett MG, Hummel D, Eschenbach DA, Holmes KK. Preterm labor associated with subclinical amniotic fluid infection and with bacterial vaginosis. Obstet Gynecol. 1986;67(2):229-237. doi:10.1097/00006250-198602000-00013. PubMed PMID: 3003634.
Moran DJ, Payne A. Subclinical intra-amniotic infection with Gardnerella vaginalis associated with preterm delivery. Case report. Br J Obstet Gynaecol. 1989;96(4):489-490. doi:10.1111/j.1471-0528.1989.tb02430.x. PubMed PMID: 2787667.
Platt MS. Neonatal Hemophilus vaginalis (Corynebacterium vaginalis) infection. Clin Pediatr (Phila). 1971;10(9):513-516. doi:10.1177/000992287101000907. PubMed PMID: 5095161.
Elovitz MA, Mrinalini C. Animal models of preterm birth. Trends Endocrinol Metab. 2004;15(10):479-487. doi:10.1016/j.tem.2004.10.009. PubMed PMID: 15541647.
Jefferson KK. The bacterial etiology of preterm birth. Adv Appl Microbiol. 2012;80:1-22. doi:10.1016/B978-0-12-394381-1.00001-5. PubMed PMID: 22794142.
Romero R, Gomez-Lopez N, Winters AD, et al. Evidence that intra-amniotic infections are often the result of an ascending invasion - a molecular microbiological study. J Perinat Med. 2019;47(9):915-931. doi:10.1515/jpm-2019-0297. PubMed PMID: 31693497; PMCID: PMC7147941.
Taylor-Robinson D. The bacteriology of Gardnerella vaginalis. Scand J Urol Nephrol Suppl. 1984;86:41-55. PubMed PMID: 6399409.
Garlind A, Pahlsson C, Forsum U. Phenotypic complexity in Mobiluncus. APMIS. 1989;97(1):38-42. PubMed PMID: 2914104.
Lawson PA, Moore E, Falsen E. Prevotella amnii sp. nov., isolated from human amniotic fluid. Int J Syst Evol Microbiol. 2008;58(1):89-92. doi:10.1099/ijs.0.65118-0. PubMed PMID: 18175689.
Anton L, Ferguson B, Friedman ES, Gerson KD, Brown AG, Elovitz MA. Gardnerella vaginalis alters cervicovaginal epithelial cell function through microbe-specific immune responses. Microbiome. 2022;10(1):119. doi:10.1186/s40168-022-01317-. Epub 20220804. PubMed PMID: 35922830; PMCID: PMC9351251.
Anton L, Sierra LJ, DeVine A, et al. Common cervicovaginal microbial supernatants alter cervical epithelial function: mechanisms by which Lactobacillus crispatus contributes to cervical health. Front Microbiol. 2018;9:2181. doi:10.3389/fmicb.2018.02181. Epub 20181008. PubMed PMID: 30349508; PMCID: PMC6186799.
Dude CM, Saylany A, Brown A, Elovitz M, Anton L. Microbial supernatants from Mobiluncus mulieris, a bacteria strongly associated with spontaneous preterm birth, disrupts the cervical epithelial barrier through inflammatory and miRNA mediated mechanisms. Anaerobe. 2020;61:102127. doi:10.1016/j.anaerobe.2019.102127. Epub 20191121. PubMed PMID: 31760081.
Burd I, Brown A, Gonzalez JM, Chai J, Elovitz MA. A mouse model of term chorioamnionitis: unraveling causes of adverse neurological outcomes. Reprod Sci. 2011;18(9):900-907. doi:10.1177/1933719111398498. Epub 20110318. PubMed PMID: 21421895; PMCID: PMC3343123.
Elovitz MA, Brown AG, Breen K, Anton L, Maubert M, Burd I. Intrauterine inflammation, insufficient to induce parturition, still evokes fetal and neonatal brain injury. Int J Dev Neurosci. 2011;29(6):663-671. doi:10.1016/j.ijdevneu.2011.02.011. Epub 20110304. PubMed PMID: 21382466; PMCID: PMC3140629.
Elovitz MA, Wang Z, Chien EK, Rychlik DF, Phillippe M. A new model for inflammation-induced preterm birth: the role of platelet-activating factor and Toll-like receptor-4. Am J Pathol. 2003;163(5):2103-2111. doi:10.1016/S0002-9440(10)63567-5. PubMed PMID: 14578208; PMCID: PMC1892431.
Elovitz MA, Mrinalini C, Sammel MD. Elucidating the early signal transduction pathways leading to fetal brain injury in preterm birth. Pediatr Res. 2006;59(1):50-55. doi:10.1203/01.pdr.0000191141.21932.b6. Epub 20051202. PubMed PMID: 16327009.
Burd I, Chai J, Gonzalez J, et al. Beyond white matter damage: fetal neuronal injury in a mouse model of preterm birth. Am J Obstet Gynecol. 2009;201(3):279. doi:10.1016/j.ajog.2009.06.013. e1-8. PubMed PMID: 19733279; PMCID: PMC2740757.
Motomura K, Romero R, Xu Y, et al. Intra-amniotic infection with ureaplasma parvum causes preterm birth and neonatal mortality that are prevented by treatment with clarithromycin. mBio. 2020;11(3):e00797-20. doi:10.1128/mBio.00797-20. Epub 20200623. PubMed PMID: 32576673; PMCID: PMC7315120.
Novy MJ, Duffy L, Axthelm MK, et al. Ureaplasma parvum or Mycoplasma hominis as sole pathogens cause chorioamnionitis, preterm delivery, and fetal pneumonia in rhesus macaques. Reprod Sci. 2009;16(1):56-70. doi:10.1177/1933719108325508. Epub 20090102. PubMed PMID: 19122105.
Fidel P, Ghezzi F, Romero R, et al. The effect of antibiotic therapy on intrauterine infection-induced preterm parturition in rabbits. J Matern Fetal Neonatal Med. 2003;14(1):57-64. doi:10.1080/jmf.14.1.57.64. PubMed PMID: 14563094.
Cappelletti M, Presicce P, Feiyang M, et al. The induction of preterm labor in rhesus macaques is determined by the strength of immune response to intrauterine infection. PLoS Biol. 2021;19(9):e3001385. doi:10.1371/journal.pbio.3001385. Epub 20210908. PubMed PMID: 34495952; PMCID: PMC8452070.
Hirsch E, Saotome I, Hirsh D. A model of intrauterine infection and preterm delivery in mice. Am J Obstet Gynecol. 1995;172(5):1598-1603. doi:10.1016/0002-9378(95)90503-0. PubMed PMID: 7538729.
Cools P. The role of Escherichia coli in reproductive health: state of the art. Res Microbiol. 2017;168(9-10):892-901. doi:10.1016/j.resmic.2017.02.002. Epub 20170224. PubMed PMID: 28242352.
Gibbs RS, McDuffie RS Jr, Kunze M, et al. Experimental intrauterine infection with Prevotella bivia in New Zealand White rabbits. Am J Obstet Gynecol. 2004;190(4):1082-1086. doi:10.1016/j.ajog.2003.10.700. PubMed PMID: 15118646.
Cheah FC, Lai CH, Tan GC, et al. Intrauterine Gardnerella vaginalis infection results in fetal growth restriction and alveolar septal hypertrophy in a rabbit model. Front Pediatr. 2020;8:593802. doi:10.3389/fped.2020.593802. Epub 20210122. PubMed PMID: 33553066; PMCID: PMC7862757.
Field NT, Newton ER, Kagan-Hallet K, Peairs WA. Perinatal effects of Gardnerella vaginalis deciduitis in the rabbit. Am J Obstet Gynecol. 1993;168(3):988-994. doi:10.1016/s0002-9378(12)90858-3. Pt 1. PubMed PMID: 8456914.
McDuffie RS Jr, Kunze M, Barr J, et al. Chronic intrauterine and fetal infection with Gardnerella vaginalis. Am J Obstet Gynecol. 2002;187(5):1263-1266. doi:10.1067/mob.2002.127129. PubMed PMID: 12439517.
Mussalli GM, Blanchard R, Brunnert SR, Hirsch E. Inflammatory cytokines in a murine model of infection-induced preterm labor: cause or effect? J Soc Gynecol Investig. 1999;6(4):188-195. doi:10.1016/s1071-5576(99)00013-1. PubMed PMID: 10486780.
Yang Q, El-Sayed Y, Rosenberg-Hasson Y, et al. Multiple cytokine profile in plasma and amniotic fluid in a mouse model of pre-term labor. Am J Reprod Immunol. 2009;62(5):339-347. doi:10.1111/j.1600-0897.2009.00743.x. PubMed PMID: 19811468.
Koga K, Mor G. Toll-like receptors at the maternal-fetal interface in normal pregnancy and pregnancy disorders. Am J Reprod Immunol. 2010;63(6):587-600. doi:10.1111/j.1600-0897.2010.00848.x. Epub 20100329. PubMed PMID: 20367625; PMCID: PMC3025804.
Underwood MA, Gilbert WM, Sherman MP. Amniotic fluid: not just fetal urine anymore. J Perinatol. 2005;25(5):341-348. doi:10.1038/sj.jp.7211290. PubMed PMID: 15861199.
Jung E, Romero R, Yeo L, et al. The fetal inflammatory response syndrome: the origins of a concept, pathophysiology, diagnosis, and obstetrical implications. Semin Fetal Neonatal Med. 2020;25(4):101146. doi:10.1016/j.siny.2020.101146. Epub 20201023. PubMed PMID: 33164775.
Romero R, Chaiworapongsa T, Espinoza J. Micronutrients and intrauterine infection, preterm birth and the fetal inflammatory response syndrome. J Nutr. 2003;133(5):1668S-73. doi:10.1093/jn/133.5.1668S. Suppl 2. PubMed PMID: 12730483.
Dinarello CA. Infection, fever, and exogenous and endogenous pyrogens: some concepts have changed. J Endotoxin Res. 2004;10(4):201-222. doi:10.1179/096805104225006129. PubMed PMID: 15373964.
Gelber SE, Aguilar JL, Lewis KL, Ratner AJ. Functional and phylogenetic characterization of Vaginolysin, the human-specific cytolysin from Gardnerella vaginalis. J Bacteriol. 2008;190(11):3896-3903. doi:10.1128/JB.01965-07. Epub 20080404. PubMed PMID: 18390664; PMCID: PMC2395025.
Randis TM, Zaklama J, LaRocca TJ, et al. Vaginolysin drives epithelial ultrastructural responses to Gardnerella vaginalis. Infect Immun. 2013;81(12):4544-4550. doi:10.1128/IAI.00627-13. Epub 20130930. PubMed PMID: 24082080; PMCID: PMC3837968.
Amabebe E, Anumba DOC. Mechanistic insights into immune suppression and evasion in bacterial vaginosis. Curr Microbiol. 2022;79(3):84. doi:10.1007/s00284-022-02771-2. Epub 20220207. PubMed PMID: 35128579; PMCID: PMC8818625.
Dada T, Rosenzweig JM, Al Shammary M, et al. Mouse model of intrauterine inflammation: sex-specific differences in long-term neurologic and immune sequelae. Brain Behav Immun. 2014;38:142-150. doi:10.1016/j.bbi.2014.01.014. Epub 20140131. PubMed PMID: 24486323; PMCID: PMC3989501.
Migale R, Herbert BR, Lee YS, et al. Specific lipopolysaccharide serotypes induce differential maternal and neonatal inflammatory responses in a murine model of preterm labor. Am J Pathol. 2015;185(9):2390-2401. doi:10.1016/j.ajpath.2015.05.015. Epub 20150726. PubMed PMID: 26212908; PMCID: PMC4597270.
Bonney EA. Demystifying animal models of adverse pregnancy outcomes: touching bench and bedside. Am J Reprod Immunol. 2013;69(6):567-584. doi:10.1111/aji.12102. Epub 20130228. PubMed PMID: 23448345; PMCID: PMC4301576.
Mitchell BF, Taggart MJ. Are animal models relevant to key aspects of human parturition? Am J Physiol Regul Integr Comp Physiol. 2009;297(3):R525-45. doi:10.1152/ajpregu.00153.2009. Epub 20090610. PubMed PMID: 19515978.
Sierra LJ, Brown AG, Barila GO, et al. Colonization of the cervicovaginal space with Gardnerella vaginalis leads to local inflammation and cervical remodeling in pregnant mice. PLoS One. 2018;13(1):e0191524. doi:10.1371/journal.pone.0191524. Epub 20180118. PubMed PMID: 29346438; PMCID: PMC5773211.
Tantengco OAG, Kechichian T, Vincent KL, Pyles RB, Medina PMB, Menon R. Inflammatory response elicited by Ureaplasma parvum colonization in human cervical epithelial, stromal, and immune cells. Reproduction. 2021;163(1):1-10. doi:10.1530/REP-21-0308. Epub 20211209. PubMed PMID: 34780348; PMCID: PMC8669769.