Women and Their Microbes: The Unexpected Friendship

Trends in Microbiology

Volumn 26, Issue 1, 2018, Pages 16-32

  Younes, Jessica A ^a   Lievens, Elke ^b,c   Hummelen, Ruben ^d   van der Westen, Rebecca ^e   Reid, Gregor ^f,g   Petrova, Mariya I ^b,c  

^a WINCLOVE PROBIOTICS   (Netherlands)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c UNIVERSITY OF ANTWERP   (Belgium)

^d MCMASTER UNIVERSITY   (Canada)

^e UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^f LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^g UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

birth; conception; menopause; microbial inheritance; pregnancy; probiotics; reproductive microbiome; urogenital health; women's health

Indexed keywords

BACTERIUM TRANSDUCTION; BIOFILM; BIOSIS; CHILD HEALTH; CHILDBIRTH; CONCEPTION; DYSBIOSIS; FEMALE; FERTILIZATION; HUMAN; LACTOBACILLUS; MATERNAL INHERITANCE; MICROBIAL COMMUNITY; NONHUMAN; OBSTETRIC DELIVERY; PREGNANCY; PRIORITY JOURNAL; REPRODUCTION; REPRODUCTIVE FITNESS; REVIEW; VAGINA FLORA; VAGINITIS; BREAST; FALLOPIAN TUBE; GASTROINTESTINAL TRACT; HEALTH; IMMUNOLOGY; INFANT; INTESTINE FLORA; MALE; MICROBIOLOGY; MICROFLORA; PHYSIOLOGY; PLACENTA; REPRODUCTIVE HEALTH; UTERUS; VAGINA;

PROBIOTIC AGENT;

BIOFILMS; BREAST; DYSBIOSIS; FALLOPIAN TUBES; FEMALE; FERTILIZATION; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HEALTH; HUMANS; INFANT; INFANT HEALTH; MALE; MICROBIOTA; PLACENTA; PREGNANCY; PROBIOTICS; REPRODUCTIVE HEALTH; UTERUS; VAGINA;

EID: 85028084936     PISSN: 0966842X     EISSN: 18784380     Source Type: Journal    
DOI: 10.1016/j.tim.2017.07.008     Document Type: Review

References (136)

1. Gilbert, S.F., et al. A symbiotic view of life: we have never been individuals. Q. Rev. Biol. 87 (2012), 325–341.
2. Bordenstein, S.R., Theis, K.R., Host biology in light of the microbiome: ten principles of holobionts and hologenomes. PLoS Biol., 13, 2015, e1002226.
3. Reid, G., Cervicovaginal microbiomes – threats and possibilities. Trends Endocrinol. Metab. 27 (2016), 446–454.
4. Petrova, M.I., et al. Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front. Physiol., 6, 2015, 81.
5. Ravel, J., et al. Vaginal microbiome of reproductive-age women. Proc. Natl. Acad. Sci. U. S. A. 1 (2011), 4680–4687.
6. van de Wijgert, J.H., et al. The vaginal microbiota: what have we learned after a decade of molecular characterization?. PLoS One, 9, 2014, e105998.
7. Macklaim, J.M., et al. At the crossroads of vaginal health and disease, the genome sequence of Lactobacillus iners AB-1. Proc. Natl. Acad. Sci. U. S. A. 108:Suppl. 1 (2011), 4688–4695.
8. Mendes-Soares, H., et al. Comparative functional genomics of Lactobacillus spp. reveals possible mechanisms for specialization of vaginal lactobacilli to their environment. J. Bacteriol. 196 (2014), 1458–1470.
9. 2. PLoS One, 9, 2014, e107758.
10. Juarez Tomas, M.S., et al. Growth and lactic acid production by vaginal Lactobacillus acidophilus CRL 1259, and inhibition of uropathogenic Escherichia coli. J. Med. Microbiol. 52 (2003), 1117–1124.
11. Graver, M.A., Wade, J.J., The role of acidification in the inhibition of Neisseria gonorrhoeae by vaginal lactobacilli during anaerobic growth. Ann. Clin. Microbiol. Antimicrob., 10, 2011, 8.
12. Conti, C., et al. Inhibition of herpes simplex virus type 2 by vaginal lactobacilli. J. Physiol. Pharmacol. 60:Suppl. 6 (2009), 19–26.
13. Shukair, S.A., et al. Human cervicovaginal mucus contains an activity that hinders HIV-1 movement. Mucosal Immunol. 6 (2013), 427–434.
14. Sgibnev, A., Kremleva, E., Influence of hydrogen peroxide, lactic acid, and surfactants from vaginal lactobacilli on the antibiotic sensitivity of opportunistic bacteria. Probiotics Antimicrob. Proteins 9 (2016), 131–141.
15. Srinivasan, U., et al. Vaginal and oral microbes, host genotype and preterm birth. Med. Hypotheses 73 (2009), 963–975.
16. Osset, J., et al. Assessment of the capacity of Lactobacillus to inhibit the growth of uropathogens and block their adhesion to vaginal epithelial cells. J. Infect. Dis. 183 (2001), 485–491.
17. Mastromarino, P., et al. Characterization and selection of vaginal Lactobacillus strains for the preparation of vaginal tablets. J. Appl. Microbiol. 93 (2002), 884–893.
18. Zarate, G., Nader-Macias, M.E., Influence of probiotic vaginal lactobacilli on in vitro adhesion of urogenital pathogens to vaginal epithelial cells. Lett. Appl. Microbiol. 43 (2006), 174–180.
19. Phukan, N., et al. The adherence of Trichomonas vaginalis to host ectocervical cells is influenced by lactobacilli. Sex. Transm. Infect. 89 (2013), 455–459.
20. Ma, B., et al. Vaginal microbiome: rethinking health and disease. Annu. Rev. Microbiol. 66 (2012), 371–389.
21. Simhan, H.N., et al. The vaginal inflammatory milieu and the risk of early premature preterm rupture of membranes. Am. J. Obstet. Gynecol. 192 (2005), 213–218.
22. Swidsinski, A., et al. An adherent Gardnerella vaginalis biofilm persists on the vaginal epithelium after standard therapy with oral metronidazole. Am. J. Obstet. Gynecol. 198 (2008), 97–106.
23. Harwich, M.D. Jr., et al. Drawing the line between commensal and pathogenic Gardnerella vaginalis through genome analysis and virulence studies. BMC Genomics, 11, 2010, 375.
24. Schellenberg, J.J., et al. Gardnerella vaginalis subgroups defined by cpn60 sequencing and sialidase activity in isolates from Canada, Belgium and Kenya. PLoS One, 11, 2016, e0146510.
25. Hardy, L., et al. A fruitful alliance: the synergy between Atopobium vaginae and Gardnerella vaginalis in bacterial vaginosis-associated biofilm. Sex. Transm. Infect. 92 (2016), 487–491.
26. van der Veer, C., The cervicovaginal microbiota in women notified for Chlamydia trachomatis infection: a case-control study at the sexually transmitted infection outpatient clinic in Amsterdam, The Netherlands. Clin. Infect. Dis. 64 (2016), 24–31.
27. Marrazzo, J.M., et al. Extravaginal reservoirs of vaginal bacteria as risk factors for incident bacterial vaginosis. J. Infect. Dis. 205 (2012), 1580–1588.
28. Castro, J., et al. Escherichia coli and Enterococcus faecalis are able to incorporate and enhance a pre-formed Gardnerella vaginalis biofilm. Pathog. Dis., 74, 2016, ftw007.
29. Machado, A., Cerca, N., Influence of biofilm formation by Gardnerella vaginalis and other anaerobes on bacterial vaginosis. J. Infect. Dis. 212 (2015), 1856–1861.
30. Patterson, J.L., et al. Effect of biofilm phenotype on resistance of Gardnerella vaginalis to hydrogen peroxide and lactic acid. Am. J. Obstet. Gynecol. 197 (2007), 170–177.
31. Fichorova, R.N., et al. The villain team-up or how Trichomonas vaginalis and bacterial vaginosis alter innate immunity in concert. Sex. Transm. Infect. 89 (2013), 460–466.
32. Kyongo, J.K., et al. Searching for lower female genital tract soluble and cellular biomarkers: defining levels and predictors in a cohort of healthy Caucasian women. PLoS One, 7, 2012, e43951.
33. Nikolaitchouk, N., et al. The lower genital tract microbiota in relation to cytokine-, SLPI- and endotoxin levels: application of checkerboard DNA–DNA hybridization (CDH). APMIS 116 (2008), 263–277.
34. Balkus, J., et al. Effects of pregnancy and bacterial vaginosis on proinflammatory cytokine and secretory leukocyte protease inhibitor concentrations in vaginal secretions. J. Pregnancy, 2010, 2010, 385981.
35. Dezzutti, C.S., et al. Performance of swabs, lavage, and diluents to quantify biomarkers of female genital tract soluble mucosal mediators. PLoS One, 6, 2011, e23136.
36. Doerflinger, S.Y., et al. Bacteria in the vaginal microbiome alter the innate immune response and barrier properties of the human vaginal epithelia in a species-specific manner. J. Infect. Dis. 209 (2014), 1989–1999.
37. Borgdorff, H., et al. Cervicovaginal microbiome dysbiosis is associated with proteome changes related to alterations of the cervicovaginal mucosal barrier. Mucosal Immunol. 9 (2016), 621–633.
38. Mitchell, C., Marrazzo, J., Bacterial vaginosis and the cervicovaginal immune response. Am. J. Reprod. Immunol. 71 (2014), 555–563.
39. Rose, W.A., et al. Commensal bacteria modulate innate immune responses of vaginal epithelial cell multilayer cultures. PLoS One, 7, 2012, e32728.
40. Fichorova, R.N., et al. Baseline variation and associations between subject characteristics and five cytokine biomarkers of vaginal safety among healthy non-pregnant women in microbicide trials. Cytokine 55 (2011), 134–140.
41. Fichorova, R.N., et al. A quantitative multiplex nuclease protection assay reveals immunotoxicity gene expression profiles in the rabbit model for vaginal drug safety evaluation. Toxicol. Appl. Pharmacol. 285 (2015), 198–206.
42. Mandar, R., et al. Complementary seminovaginal microbiome in couples. Res. Microbiol. 166 (2015), 440–447.
43. Hou, D., et al. Microbiota of the seminal fluid from healthy and infertile men. Fertil. Steril. 100 (2013), 1261–1269.
44. Jarvi, K., et al. Polymerase chain reaction-based detection of bacteria in semen. Fertil. Steril. 66 (1996), 463–467.
45. Kiessling, A.A., et al. Detection and identification of bacterial DNA in semen. Fertil. Steril. 90 (2008), 1744–1756.
46. Mandar, R., et al. Seminal microbiome in men with and without prostatitis. Int. J. Urol. 24 (2017), 211–216.
47. Weng, S.L., et al. Bacterial communities in semen from men of infertile couples: metagenomic sequencing reveals relationships of seminal microbiota to semen quality. PLoS One, 9, 2014, e110152.
48. Barbonetti, A., et al. Effect of vaginal probiotic lactobacilli on in vitro-induced sperm lipid peroxidation and its impact on sperm motility and viability. Fertil. Steril. 95 (2011), 2485–2488.
49. Barbonetti, A., et al. Soluble products of Escherichia coli induce mitochondrial dysfunction-related sperm membrane lipid peroxidation which is prevented by lactobacilli. PLoS One, 8, 2013, e83136.
50. Zozaya, M., et al. Bacterial communities in penile skin, male urethra, and vaginas of heterosexual couples with and without bacterial vaginosis. Microbiome, 4, 2016, 16.
51. Hyman, R.W., et al. The dynamics of the vaginal microbiome during infertility therapy with in vitro fertilization-embryo transfer. J. Assist. Reprod. Genet. 29 (2012), 105–115.
52. Salah, R.M., et al. Bacterial vaginosis and infertility: cause or association?. Eur. J. Obstet. Gynecol. Reprod. Biol. 167 (2013), 59–63.
53. van Oostrum, N., et al. Risks associated with bacterial vaginosis in infertility patients: a systematic review and meta-analysis. Hum. Reprod. 28 (2013), 1809–1815.
54. Haahr, T., et al. Abnormal vaginal microbiota may be associated with poor reproductive outcomes: a prospective study in IVF patients. Hum. Reprod. 31 (2016), 795–803.
55. Pelzer, E.S., et al. Microorganisms within human follicular fluid: effects on IVF. PLoS One, 8, 2013, e59062.
56. Franasiak, J.M., et al. Endometrial microbiome at the time of embryo transfer: next-generation sequencing of the 16S ribosomal subunit. J. Assist. Reprod. Genet. 33 (2016), 129–136.
57. Verstraelen, H., et al. Characterisation of the human uterine microbiome in non-pregnant women through deep sequencing of the V1-2 region of the 16S rRNA gene. PeerJ, 4, 2016, e1602.
58. Moreno, I., et al. Evidence that the endometrial microbiota has an effect on implantation success or failure. Am. J. Obstet. Gynecol. 215 (2016), 684–703.
59. Robertson, S.A., Immune regulation of conception and embryo implantation – all about quality control?. J. Reprod. Immunol. 85 (2010), 51–57.
60. Sisti, G., et al. Maternal immunity and pregnancy outcome: focus on preconception and autophagy. Genes Immun. 17 (2016), 1–7.
61. Aagaard, K., et al. The placenta harbors a unique microbiome. Sci. Transl. Med., 6, 2014, 237ra65.
62. Rautava, S., et al. Probiotics modulate host–microbe interaction in the placenta and fetal gut: a randomized, double-blind, placebo-controlled trial. Neonatology 102 (2012), 178–184.
63. Zaura, E., et al. Acquiring and maintaining a normal oral microbiome: current perspective. Front. Cell. Infect. Microbiol., 4, 2014, 85.
64. Prince, A., The bitter taste of infection. J. Clin. Invest. 122 (2012), 3847–3849.
65. Koren, O., et al. Host remodeling of the gut microbiome and metabolic changes during pregnancy. Cell 150 (2012), 470–480.
66. Fujiwara, N., et al. Significant increase of oral bacteria in the early pregnancy period in Japanese women. J. Invest. Clin. Dent., 8, 2017, 10.
67. Collado, M.C., et al. Human gut colonisation may be initiated in utero by distinct microbial communities in the placenta and amniotic fluid. Sci. Rep., 6, 2016, 23129.
68. Jimenez, E., et al. Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr. Microbiol. 51 (2005), 270–274.
69. Makino, H., et al. Transmission of intestinal Bifidobacterium longum subsp. longum strains from mother to infant, determined by multilocus sequencing typing and amplified fragment length polymorphism. Appl. Environ. Microbiol. 77 (2011), 6788–6793.
70. Makino, H., et al. Mother-to-infant transmission of intestinal bifidobacterial strains has an impact on the early development of vaginally delivered infant's microbiota. PLoS One, 8, 2013, e78331.
71. Christian, P., et al. Prenatal micronutrient supplementation and intellectual and motor function in early school-aged children in Nepal. JAMA 304 (2010), 2716–2723.
72. Chang, C.Y., et al. Essential fatty acids and human brain. Acta Neurol. Taiwan. 18 (2009), 231–241.
73. Ogawa, J., et al. Production of conjugated fatty acids by lactic acid bacteria. J. Biosci. Bioeng. 100 (2005), 355–364.
74. Rossi, M., et al. Folate production by probiotic bacteria. Nutrients 3 (2011), 118–134.
75. Ganguli, K., et al. Lactobacillus rhamnosus GG and its SpaC pilus adhesin modulate inflammatory responsiveness and TLR-related gene expression in the fetal human gut. Pediatr. Res. 77 (2015), 528–535.
76. Janvier, A., et al. Cohort study of probiotics in a North American neonatal intensive care unit. J. Pediatr. 164 (2014), 980–985.
77. Ilmonen, J., et al. Impact of dietary counselling and probiotic intervention on maternal anthropometric measurements during and after pregnancy: a randomized placebo-controlled trial. Clin. Nutr. 30 (2011), 156–164.
78. Laitinen, K., et al. Probiotics and dietary counselling contribute to glucose regulation during and after pregnancy: a randomised controlled trial. Br. J. Nutr. 101 (2009), 1679–1687.
79. Luoto, R., et al. Impact of maternal probiotic-supplemented dietary counseling during pregnancy on colostrum adiponectin concentration: a prospective, randomized, placebo-controlled study. Early Hum. Dev. 88 (2012), 339–344.
80. Huurre, A., et al. Impact of maternal atopy and probiotic supplementation during pregnancy on infant sensitization: a double-blind placebo-controlled study. Clin. Exp. Allergy 38 (2008), 1342–1348.
81. Kukkonen, K., et al. Probiotics and prebiotic galacto-oligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J. Allergy Clin. Immunol. 119 (2007), 192–198.
82. Tremaroli, V., et al. Roux-en-Y gastric bypass and vertical banded gastroplasty induce long-term changes on the human gut microbiome contributing to fat mass regulation. Cell Metab. 22 (2015), 228–238.
83. Vrieze, A., et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143 (2012), 913–916.
84. Lindsay, K.L., et al. Probiotics in obese pregnancy do not reduce maternal fasting glucose: a double-blind, placebo-controlled, randomized trial (Probiotics in Pregnancy Study). Am. J. Clin. Nutr. 99 (2014), 1432–1439.
85. Neish, A.S., Microbes in gastrointestinal health and disease. Gastroenterology 136 (2009), 65–80.
86. Rijkers, G.T., et al. Guidance for substantiating the evidence for beneficial effects of probiotics: current status and recommendations for future research. J. Nutr. 140 (2010), 671S–676S.
87. Mueller, N.T., et al. The infant microbiome development: mom matters. Trends Mol. Med. 21 (2015), 109–117.
88. Mueller, N.T., et al. Prenatal exposure to antibiotics, cesarean section and risk of childhood obesity. Int. J. Obes. (Lond) 39 (2015), 665–670.
89. Cox, L.M., et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell 158 (2014), 705–721.
90. Dominguez-Bello, M.G., et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 11971–11975.
91. Bonifacio, E., et al. Cesarean section and interferon-induced helicase gene polymorphisms combine to increase childhood type 1 diabetes risk. Diabetes 60 (2011), 3300–3306.
92. Cardwell, C.R., et al. Caesarean section is associated with an increased risk of childhood-onset type 1 diabetes mellitus: a meta-analysis of observational studies. Diabetologia 51 (2008), 726–735.
93. Li, H.T., et al. The impact of cesarean section on offspring overweight and obesity: a systematic review and meta-analysis. Int. J. Obes. (Lond) 37 (2013), 893–899.
94. Ridaura, V.K., et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science, 341, 2013, 1241214.
95. Mueller, N.T., et al. Birth mode-dependent association between pre-pregnancy maternal weight status and the neonatal intestinal microbiome. Sci. Rep., 6, 2016, 23133.
96. Collado, M.C., et al. Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. Am. J. Clin. Nutr. 88 (2008), 894–899.
97. Collado, M.C., et al. Effect of mother's weight on infant's microbiota acquisition, composition, and activity during early infancy: a prospective follow-up study initiated in early pregnancy. Am. J. Clin. Nutr. 92 (2010), 1023–1030.
98. Galley, J.D., et al. Maternal obesity is associated with alterations in the gut microbiome in toddlers. PLoS One, 9, 2014, e113026.
99. Martin, R., et al. Early-life events, including mode of delivery and type of feeding, siblings and gender, shape the developing gut Microbiota. PLoS One, 11, 2016, e0158498.
100. Dominguez-Bello, M.G., et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat. Med. 22 (2016), 250–253.
101. Cunnington, A.J., et al. ‘Vaginal seeding’ of infants born by caesarean section. BMJ, 352, 2016, i227.
102. Clemente, J.C., Dominguez-Bello, M.G., Safety of vaginal microbial transfer in infants delivered by caesarean, and expected health outcomes. BMJ, 352, 2016, i1707.
103. Jost, T., et al. Impact of human milk bacteria and oligosaccharides on neonatal gut microbiota establishment and gut health. Nutr. Rev. 73 (2015), 426–437.
104. Urbaniak, C., et al. Human milk microbiota profiles in relation to birthing method, gestation and infant gender. Microbiome, 4, 2016, 1.
105. Soto, A., et al. Lactobacilli and bifidobacteria in human breast milk: influence of antibiotherapy and other host and clinical factors. J. Pediatr. Gastroenterol. Nutr. 59 (2014), 78–88.
106. Cabrera-Rubio, R., et al. The human milk microbiome changes over lactation and is shaped by maternal weight and mode of delivery. Am. J. Clin. Nutr. 96 (2012), 544–551.
107. Urbaniak, C., et al. Effect of chemotherapy on the microbiota and metabolome of human milk, a case report. Microbiome, 2, 2014, 24.
108. Bezirtzoglou, E., et al. Microbiota profile in feces of breast- and formula-fed newborns by using fluorescence in situ hybridization (FISH). Anaerobe 17 (2011), 478–482.
109. Backhed, F., et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe 17 (2015), 690–703.
110. Bevins, C.L., Salzman, N.H., The potter's wheel: the host's role in sculpting its microbiota. Cell. Mol. Life Sci. 68 (2011), 3675–3685.
111. Blekhman, R., et al. Host genetic variation impacts microbiome composition across human body sites. Genome Biol., 16, 2015, 191.
112. Goodrich, J.K., et al. Cross-species comparisons of host genetic associations with the microbiome. Science 352 (2016), 532–535.
113. Knights, D., et al. Complex host genetics influence the microbiome in inflammatory bowel disease. Genome Med., 6, 2014, 107.
114. Goodrich, J.K., et al. Human genetics shape the gut microbiome. Cell 159 (2014), 789–799.
115. Ley, R.E., The gene–microbe link. Nature, 518, 2015, S7.
116. Paavonen, J., Physiology and ecology of the vagina. Scand. J. Infect. Dis. Suppl. 40 (1983), 31–35.
117. Gregoire, A.T., et al. The glycogen content of human vaginal epithelial tissue. Fertil. Steril. 22 (1971), 64–68.
118. Dei, M., et al. Vulvovaginitis in childhood. Best Pract. Res. Clin. Obstet. Gynaecol. 24 (2010), 129–137.
119. Randelovic, G., et al. Microbiological aspects of vulvovaginitis in prepubertal girls. Eur. J. Pediatr. 171 (2012), 1203–1208.
120. Yamamoto, T., et al. Bacterial populations in the vaginas of healthy adolescent women. J. Pediatr. Adolesc. Gynecol. 22 (2009), 11–18.
121. Gupta, S., et al. Vaginal microflora in postmenopausal women on hormone replacement therapy. Indian J. Pathol. Microbiol. 49 (2006), 457–461.
122. Hummelen, R., et al. Vaginal microbiome and epithelial gene array in post-menopausal women with moderate to severe dryness. PLoS One, 6, 2011, e26602.
123. Bradshaw, C.S., et al. High recurrence rates of bacterial vaginosis over the course of 12 months after oral metronidazole therapy and factors associated with recurrence. J. Infect. Dis. 193 (2006), 1478–1486.
124. Donlan, R.M., Costerton, J.W., Biofilms: survival mechanisms of clinically relevant microorganisms. Clin. Microbiol. Rev. 15 (2002), 167–193.
125. Cerca, N., et al. Comparative assessment of antibiotic susceptibility of coagulase-negative staphylococci in biofilm versus planktonic culture as assessed by bacterial enumeration or rapid XTT colorimetry. J. Antimicrob. Chemother. 56 (2005), 331–336.
126. Swidsinski, A., et al. Polymicrobial Gardnerella biofilm resists repeated intravaginal antiseptic treatment in a subset of women with bacterial vaginosis: a preliminary report. Arch. Gynecol. Obstet. 291 (2015), 605–609.
127. Hardy, L., et al. Bacterial biofilms in the vagina. Res. Microbiol., 2017, 10.1016/j.resmic.2017.02.001 February 21, 2017.
128. Petrova, M.I., et al. Lectin-like molecules of Lactobacillus rhamnosus GG inhibit pathogenic Escherichia coli and Salmonella biofilm formation. PLoS One, 11, 2016, e0161337.
129. Petrova, M.I., et al. The lectin-like protein 1 in Lactobacillus rhamnosus GR-1 mediates tissue-specific adherence to vaginal epithelium and inhibits urogenital pathogens. Sci. Rep., 6, 2016, 37437.
130. Velraeds, M.M., et al. Inhibition of uropathogenic biofilm growth on silicone rubber in human urine by lactobacilli – a teleologic approach. World J. Urol. 18 (2000), 422–426.
131. Gudina, E.J., et al. Antimicrobial and antiadhesive properties of a biosurfactant isolated from Lactobacillus paracasei ssp. paracasei A20. Lett. Appl. Microbiol. 50 (2010), 419–424.
132. Urbaniak, C., et al. Microbiota of human breast tissue. Appl. Environ. Microbiol. 80 (2014), 3007–3014.
133. Urbaniak, C., et al. The microbiota of breast tissue and its association with breast cancer. Appl. Environ. Microbiol. 82 (2016), 5039–5048.
134. Xuan, C., et al. Microbial dysbiosis is associated with human breast cancer. PLoS One, 9, 2014, e83744.
135. Ma, Z.S., et al. Network analysis suggests a potentially ‘evil’ alliance of opportunistic pathogens inhibited by a cooperative network in human milk bacterial communities. Sci. Rep., 5, 2015, 8275.
136. Rescigno, M., et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2 (2001), 361–367.