The placenta harbors a unique microbiome

Science Translational Medicine

Volumn 6, Issue 237, 2014, Pages

  Aagaard, Kjersti ^a,b   Ma, Jun ^a,b   Antony, Kathleen M ^a   Ganu, Radhika ^a   Petrosino, Joseph ^b   Versalovic, James ^a  

^a TEXAS CHILDREN S HOSPITAL   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTEROIDETES; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; FIRMICUTES; FIRST TRIMESTER PREGNANCY; FUSOBACTERIA; HUMAN; INTESTINE FLORA; INTRAUTERINE INFECTION; MAJOR CLINICAL STUDY; MEDICAL HISTORY; MICROBIAL METABOLISM; MICROBIOME; MOLLICUTES; MOUTH FLORA; NONHUMAN; PLACENTA FLORA; PREMATURE LABOR; PRIORITY JOURNAL; PROTEOBACTERIA; SKIN FLORA; TAXONOMIC IDENTIFICATION; URINARY TRACT INFECTION; VAGINA FLORA;

BACTERIA; CASE-CONTROL STUDIES; CHI-SQUARE DISTRIBUTION; CLASSIFICATION; DNA, BACTERIAL; FEMALE; HUMANS; METAGENOMICS; MICROBIOTA; MULTIVARIATE ANALYSIS; PLACENTA; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PREGNANCY TRIMESTER, FIRST; PREMATURE BIRTH; RIBOTYPING; RISK FACTORS; RNA, RIBOSOMAL, 16S; URINARY TRACT INFECTIONS;

EID: 84901358163     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.3008599     Document Type: Article

References (58)

1. Human Microbiome Project Consortium, Structure, function and diversity of the healthy human microbiome. Nature 486, 207-214 (2012).
2. Human Microbiome Project Consortium, A framework for human microbiome research. Nature 486, 215-221 (2012).
3. K. Aagaard, J. Petrosino, W. Keitel, M. Watson, J. Katancik, N. Garcia, S. Patel, M. Cutting, T. Madden, H. Hamilton, E. Harris, D. Gevers, G. Simone, P. McInnes, J. Versalovic, The Human Microbiome Project strategy for comprehensive sampling of the human microbiome and why it matters. FASEB J. 27, 1012-1022 (2013).
4. K. Aagaard, K. Riehle, J. Ma, N. Segata, T. A. Mistretta, C. Coarfa, S. Raza, S. Rosenbaum, I. Van den Veyver, A. Milosavljevic, D. Gevers, C. Huttenhower, J. Petrosino, J. Versalovic, A metagenomic approach to characterization of the vaginal microbiome signature in pregnancy. PLOS One 7, e36466 (2012).
5. R. I. Mackie, A. Sghir, H. R. Gaskins, Developmental microbial ecology of the neonatal gastrointestinal tract. Am. J. Clin. Nutr. 69, 1035S-1045S (1999).
6. C. F. Favier, E. E. Vaughan, W. M. De Vos, A. D. L. Akkermans, Molecular monitoring of succession of bacterial communities in human neonates. Appl. Environ. Microbiol. 68, 219-226 (2002).
7. J. Penders, C. Thijs, C. Vink, F. F. Stelma, B. Snijders, I. Kummeling, P. A. van den Brandt, E. E. Stobberingh, Factors influencing the composition of the intestinal microbiota in early infancy. Pediatrics 118, 511-521 (2006).
8. K. Kurokawa, T. Itoh, T. Kuwahara, K. Oshima, H. Toh, A. Toyoda, H. Takami, H. Morita, V. K. Sharma, T. P. Srivastava, T. D. Taylor, H. Noguchi, H. Mori, Y. Ogura, D. S. Ehrlich, K. Itoh, T. Takagi, Y. Sakaki, T. Hayashi, M. Hattori, Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes. DNA Res. 14, 169-181 (2007).
9. C. Palmer, E. M. Bik, D. B. DiGiulio, D. A. Relman, P. O. Brown, Development of the human infant intestinal microbiota. PLOS Biol. 5, e177 (2007).
10. C. Reinhardt, C. S. Reigstad, F. Bäckhed, Intestinal microbiota during infancy and its implications for obesity. J. Pediatr. Gastroenterol. Nutr. 48, 249-256 (2009).
11. M. M. Grönlund, O. P. Lehtonen, E. Eerola, P. Kero, Fecal microflora in healthy infants born by different methods of delivery: Permanent changes in intestinal flora after cesarean delivery. J. Pediatr. Gastroenterol. Nutr. 28 19-25 (1999).
12. M. G. Dominguez-Bello, E. K. Costello, M. Contreras, M. Magris, G. Hidalgo, N. Fierer, R. Knight, 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, 11971-11975 (2010).
13. M. B. Azad, T. Konya, H. Maughan, D. S. Guttman, C. J. Field, R. S. Chari, M. R. Sears, A. B. Becker, J. A. Scott, A. L. Kozyrskyj, C. S. Investigators, Gut microbiota of healthy Canadian infants: Profiles by mode of delivery and infant diet at 4 months. CMAJ 185, 385-394 (2013).
14. P. J. Turnbaugh, M. Hamady, T. Yatsunenko, B. L. Cantarel, A. Duncan, R. E. Ley, M. L. Sogin, W. J. Jones, B. A. Roe, J. P. Affourtit, M. Egholm, B. Henrissat, A. C. Heath, R. Knight, J. I. Gordon, A core gut microbiome in obese and lean twins. Nature 457, 480-484 (2009).
15. X. Zhou, C. J. Brown, Z. Abdo, C. C. Davis, M. A. Hansmann, P. Joyce, J. A. Foster, L. J. Forney, Differences in the composition of vaginal microbial communities found in healthy Caucasian and black women. ISME J. 1, 121-133 (2007).
16. L. J. Forney, J. A. Foster, W. Ledger, The vaginal flora of healthy women is not always dominated by Lactobacillus species. J. Infect. Dis. 194, 1468-1469 (2006).
17. R. Sood, J. L. Zehnder, M. L. Druzin, P. O. Brown, Gene expression patterns in human placenta. Proc. Natl. Acad. Sci. U.S.A. 103, 5478-5483 (2006).
18. M. J. Stout, B. Conlon, M. Landeau, I. Lee, C. Bower, Q. Zhao, K. A. Roehl, D. M. Nelson, G. A. Macones, I. U. Mysorekar, Identification of intracellular bacteria in the basal plate of the human placenta in term and preterm gestations. Am. J. Obstet. Gynecol. 208, 226.e1-226.e7 (2013).
19. R. L. Goldenberg, J. C. Hauth, W. W. Andrews, Intrauterine infection and preterm delivery. N. Engl. J. Med. 342, 1500-1507 (2000).
20. R. Romero, C. Schaudinn, J. P. Kusanovic, A. Gorur, F. Gotsch, P. Webster, C. L. Nhan-Chang, O. Erez, C. J. Kim, J. Espinoza, L. F. Gonçalves, E. Vaisbuch, S. Mazaki-Tovi, S. S. Hassan, J. W. Costerton, Detection of a microbial biofilm in intraamniotic infection. Am. J. Obstet. Gynecol. 198, 135.e1-135.e5 (2008).
21. Y. Fardini, P. Chung, R. Dumm, N. Joshi, Y. W. Han, Transmission of diverse oral bacteria to murine placenta: Evidence for the oral microbiome as a potential source of intrauterine infection. Infect. Immun. 78, 1789-1796 (2010).
22. Y. W. Han, A. Ikegami, N. F. Bissada, M. Herbst, R. W. Redline, G. G. Ashmead, Transmission of an uncultivated Bergeyella strain from the oral cavity to amniotic fluid in a case of preterm birth. J. Clin. Microbiol. 44, 1475-1483 (2006).
23. Y. W. Han, Y. Fardini, C. Chen, K. G. Iacampo, V. A. Peraino, J. M. Shamonki, R. W. Redline, Term stillbirth caused by oral Fusobacterium nucleatum. Obstet. Gynecol. 115, 442-445 (2010).
24. Y. W. Han, T. Shen, P. Chung, I. A. Buhimschi, C. S. Buhimschi, Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J. Clin. Microbiol. 47, 38-47 (2009).
25. Y. Fardini, X. Wang, S. Témoin, S. Nithianantham, D. Lee, M. Shoham, Y. W. Han, Fusobacterium nucleatum adhesin FadA binds vascular endothelial cadherin and alters endothelial integrity. Mol. Microbiol. 82, 1468-1480 (2011).
26. S. Offenbacher, V. Katz, G. Fertik, J. Collins, D. Boyd, G. Maynor, R. McKaig, J. Beck, Periodontal infection as a possible risk factor for preterm low birth weight. J. Periodontol. 67, 1103-1113 (1996).
27. S. Offenbacher, J.D. Beck, H. L. Jared, S.M. Mauriello, L. C. Mendoza,D. J. Couper, D. D. Stewart, A. P. Murtha, D. L. Cochran, D. J. Dudley, M. S. Reddy, N. C. Geurs, J. C. Hauth, I. Maternal Oral Therapy to Reduce Obstetric Risk Investigators, Effects of periodontal therapy on rate of preterm delivery: A randomized controlled trial. Obstet. Gynecol. 114, 551-559 (2009).
28. B. S. Michalowicz, J. S.Hodges, A. J. DiAngelis, V. R. Lupo, M. J. Novak, J. E. Ferguson, W. Buchanan, J. Bofill, P. N. Papapanou, D. A. Mitchell, S. Matseoane, P. A. Tschida, O. P. T. Study, Treatment of periodontal disease and the risk of preterm birth. N. Engl. J. Med. 355, 1885-1894 (2006).
29. G. A. Macones, S. Parry, D. B. Nelson, J. F. Strauss, J. Ludmir, A. W. Cohen, D. M. Stamilio, D. Appleby, B. Clothier, M. D. Sammel, M. Jeffcoat, Treatment of localized periodontal disease in pregnancy does not reduce the occurrence of preterm birth: Results from the Periodontal Infections and Prematurity Study (PIPS). Am. J. Obstet. Gynecol. 202, 147.e1-147.e8 (2010).
30. J. E. Koenig, A. Spor, N. Scalfone, A. D. Fricker, J. Stombaugh, R. Knight, L. T. Angenent, R. E. Ley, Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl. Acad. Sci. U.S.A. 108 (Suppl. 1), 4578-4585 (2011).
31. L. V. Moore, J. L. Johnson, W. E. Moore, Descriptions of Prevotella tannerae sp. nov. and Prevotella enoeca sp. nov. from the human gingival crevice and emendation of the description of Prevotella zoogleoformans. Int. J. Syst. Bacteriol. 44, 599-602 (1994).
32. C. J. Adler, K. Dobney, L. S. Weyrich, J. Kaidonis, A.W. Walker, W. Haak, C. J. A. Bradshaw, G. Townsend, A. Sołtysiak, K. W. Alt, J. Parkhill, A. Cooper, Sequencing ancient calcified dental plaque shows changes in oral microbiota with dietary shifts of the Neolithic and Industrial revolutions. Nat. Genet. 45, 450 -455 (2013).
33. B. Jiang, X. Liang, Y. Chen, T. Ma, L. Liu, J. Li, R. Jiang, T. Chen, X. Zhang, S. Li, Integrating next-generation sequencing and traditional tongue diagnosis to determine tongue coating microbiome. Sci. Rep. 2, 936 (2012).
34. G. M. Nava, F. Carbonero, J. A. Croix, E. Greenberg, H. R. Gaskins, Abundance and diversity of mucosa-associated hydrogenotrophic microbes in the healthy human colon. ISME J. 6, 57-70 (2012).
35. G. M. Nava, H. J. Friedrichsen, T. S. Stappenbeck, Spatial organization of intestinal microbiota in the mouse ascending colon. ISME J. 5, 627-638 (2011).
36. D. Knights, J. Kuczynski, E. S. Charlson, J. Zaneveld, M. C. Mozer, R. G. Collman, F. D. Bushman, R. Knight, S. T. Kelley, Bayesian community-wide culture-independent microbial source tracking. Nat. Methods 8, 761-763 (2011).
37. R. M. Brotman, Vaginal microbiome and sexually transmitted infections: An epidemiologic perspective. J. Clin. Invest. 121, 4610-4617 (2011).
38. M. J. Gosalbes, S. Llop, Y. Vallès, A. Moya, F. Ballester, M. P. Francino, Meconium microbiota types dominated by lactic acid or enteric bacteria are differentially associated with maternal eczema and respiratory problems in infants. Clin. Exp. Allergy 43, 198-211 (2013).
39. X. Wang, C. S. Buhimschi, S. Temoin, V. Bhandari, Y. W. Han, I. A. Buhimschi, Comparative microbial analysis of paired amniotic fluid and cord blood from pregnancies complicated by preterm birth and early-onset neonatal sepsis. PLOS One 8, e56131 (2013).
40. J. G. Caporaso, J. Kuczynski, J. Stombaugh, K. Bittinger, F. D. Bushman, E. K. Costello, N. Fierer, A. G. Peña, J. K. Goodrich, J. I. Gordon, G. A. Huttley, S. T. Kelley, D. Knights, J. E. Koenig, R. E. Ley, C. A. Lozupone, D. McDonald, B. D. Muegge, M. Pirrung, J. Reeder, J. R. Sevinsky, P. J. Turnbaugh, W. A. Walters, J. Widmann, T. Yatsunenko, J. Zaneveld, R. Knight, QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336 (2010).
41. N. Segata, J. Izard, L. Waldron, D. Gevers, L. Miropolsky, W. S. Garrett, C. Huttenhower, Metagenomic biomarker discovery and explanation. Genome Biol. 12, R60 (2011).
42. T. Nakatsuji, H. I. Chiang, S. B. Jiang, H. Nagarajan, K. Zengler, R. L. Gallo, The microbiome extends to subepidermal compartments of normal skin. Nat. Commun. 4, 1431 (2013).
43. Y. W. Han, R. W. Redline, M. Li, L. Yin, G. B. Hill, T. S. McCormick, Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: Implication of oral bacteria in preterm birth. Infect. Immun. 72, 2272 -2279 (2004).
44. A. L. Horton, K. A. Boggess, Periodontal disease and preterm birth. Obstet. Gynecol. Clin. North Am. 39, 17- 23 (2012).
45. X. Xiong, P. Buekens, R. L. Goldenberg, S. Offenbacher, X. Qian, Optimal timing of periodontal disease treatment for prevention of adverse pregnancy outcomes: Before or during pregnancy? Am. J. Obstet. Gynecol. 205, 111.e1-111.e6 (2011).
46. Y. W. Han, Oral health and adverse pregnancy outcomes - What's next? J. Dent. Res. 90, 289-293 (2011).
47. Y. W. Han, X. Wang, Mobile microbiome: Oral bacteria in extra-oral infections and inflammation. J. Dent. Res. 92, 485-491 (2013).
48. I. U. Mysorekar, S. J. Hultgren, Mechanisms of uropathogenic Escherichia coli persistence and eradication from the urinary tract. Proc. Natl. Acad. Sci. U.S.A. 103, 14170 - 14175 (2006).
49. X. R. Wu, T. T. Sun, J. J. Medina, In vitro binding of type 1-fimbriated Escherichia coli to uroplakins Ia and Ib: Relation to urinary tract infections. Proc. Natl. Acad. Sci. U.S.A. 93, 9630-9635 (1996).
50. W. W. Andrews, J. C. Hauth, S. P. Cliver, M. G. Conner, R. L. Goldenberg, A. R. Goepfert, Association of asymptomatic bacterial vaginosis with endometrial microbial colonization and plasma cell endometritis in nonpregnant women. Am. J. Obstet. Gynecol. 195, 1611-1616 (2006).
51. L. J. Muglia, M. Katz, The enigma of spontaneous preterm birth. N. Engl. J. Med. 362, 529-535 (2010).
52. J. R. Cole, Q. Wang, E. Cardenas, J. Fish, B. Chai, R. J. Farris, A. S. Kulam-Syed-Mohideen, D. M. McGarrell, T. Marsh, G. M. Garrity, J. M. Tiedje, The Ribosomal Database Project: Improved alignments and new tools for rRNA analysis. Nucleic Acids Res. 37, D141-D145 (2009).
53. N. Segata, L. Waldron, A. Ballarini, V. Narasimhan, O. Jousson, C. Huttenhower, Metagenomic microbial community profiling using unique clade-specific marker genes. Nat. Methods 9, 811-814 (2012).
54. S. Abubucker, N. Segata, J. Goll, A. M. Schubert, J. Izard, B. L. Cantarel, B. Rodriguez-Mueller, J. Zucker, M. Thiagarajan, B. Henrissat, O. White, S. T. Kelley, B. Methé, P. D. Schloss, D. Gevers, M. Mitreva, C. Huttenhower, Metabolic reconstruction for metagenomic data and its application to the human microbiome. PLOS Comput. Biol. 8, e1002358 (2012).
55. M. Kanehisa, S. Goto, Y. Sato, M. Furumichi, M. Tanabe, KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40, D109-D114 (2012).
56. E. M. Glass, J. Wilkening, A. Wilke, D. Antonopoulos, F. Meyer, Using the metagenomics RAST server (MG-RAST) for analyzing shotgun metagenomes. Cold Spring Harb. Protoc. 2010, pdb.prot5368 (2010).
57. Y. Ye, Identification and quantification of abundant species from pyrosequences of 16S rRNA by consensus alignment. Proc. IEEE Int. Conf. Bioinformatics Biomed. 2010, 153 -157 (2011).
58. B. J. Haas, D. Gevers, A. M. Earl, M. Feldgarden, D. V. Ward, G. Giannoukos, D. Ciulla, D. Tabbaa, S. K. Highlander, E. Sodergren, B. Methé, T. Z. DeSantis; Human Microbiome Consortium, J. F. Petrosino, R. Knight, B. W. Birren, Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21, 494-504 (2011).