Fusobacterium nucleatum and adverse pregnancy outcomes: Epidemiological and mechanistic evidence

Anaerobe

Volumn 50, Issue , 2018, Pages 55-59

  Vander Haar, Emilie L ^a   So, Jeewon ^b   Gyamfi Bannerman, Cynthia ^a   Han, Yiping W ^a,b  

^a Department of Medicine   (United States)

^b New York Presbyterian Columbia University Medical Center   (United States)

Author keywords

Chorioamnionitis; FadA; Fusobacterium nucleatum; Neonatal sepsis; Oral anaerobe; Placenta; Pregnancy complications; Preterm birth; Stillbirth; VE cadherin

Indexed keywords

ADVERSE OUTCOME; BACTERIAL VIRULENCE; CHORIOAMNIONITIS; FUSOBACTERIUM INFECTION; FUSOBACTERIUM NUCLEATUM; HUMAN; NEWBORN SEPSIS; NONHUMAN; PATHOGENESIS; PERIODONTAL DISEASE; PREECLAMPSIA; PREGNANCY OUTCOME; PREMATURE FETUS MEMBRANE RUPTURE; PREMATURE LABOR; PRIORITY JOURNAL; REVIEW; STILLBIRTH; ANIMAL; COMPLICATION; FEMALE; MICROBIOLOGY; MOUTH MUCOSA; PATHOGENICITY; PREGNANCY; PREGNANCY COMPLICATION; VIRULENCE;

ANIMALS; FEMALE; FUSOBACTERIUM INFECTIONS; FUSOBACTERIUM NUCLEATUM; HUMANS; MOUTH MUCOSA; PERIODONTAL DISEASES; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY COMPLICATIONS, INFECTIOUS; PREGNANCY OUTCOME; VIRULENCE;

EID: 85041502670     PISSN: 10759964     EISSN: 10958274     Source Type: Journal    
DOI: 10.1016/j.anaerobe.2018.01.008     Document Type: Review

References (60)

1. Goldenberg, R.L., Hauth, J.C., Andrews, W.W., Intrauterine infection and preterm delivery. N. Engl. J. Med. 342 (2000), 1500–1507.
2. Goldenberg, R.L., Thompson, C., The infectious origins of stillbirth. Am. J. Obstet. Gynecol. 189 (2003), 861–873.
3. McClure, E.M., Goldenberg, R.L., Infection and stillbirth. Semin. Fetal Neonatal Med. 14 (2009), 182–189.
4. Premature Birth Report Card, 2016, March of Dimes Perinatal Data Center.
5. McCormick, M.C., Behrman, R.E., The quiet epidemic of premature birth: commentary on a recent Institute of Medicine report. Ambul. Pediatr. 7 (2007), 8–9.
6. Sanz, M., Kornman, K., E.F.P.A.A.P.w. working group 3 of the joint, Periodontitis and adverse pregnancy outcomes: consensus report of the joint EFP/AAP workshop on periodontitis and systemic diseases. J. Periodontol. 84 (2013), S164–S169.
7. Madianos, P.N., Bobetsis, Y.A., Offenbacher, S., Adverse pregnancy outcomes (APOs) and periodontal disease: pathogenic mechanisms. J. Periodontol. 84 (2013), S170–S180.
8. Ghidini, A., Jenkins, C.B., Spong, C.Y., Pezzullo, J.C., Salafia, C.M., Eglinton, G.S., Elevated amniotic fluid interleukin-6 levels during the early second trimester are associated with greater risk of subsequent preterm delivery. Am. J. Reprod. Immunol. 37 (1997), 227–231.
9. Wenstrom, K.D., Andrews, W.W., Hauth, J.C., Goldenberg, R.L., DuBard, M.B., Cliver, S.P., Elevated second-trimester amniotic fluid interleukin-6 levels predict preterm delivery. Am. J. Obstet. Gynecol. 178 (1998), 546–550.
10. Murtha, A.P., Greig, P.C., Jimmerson, C.E., Herbert, W.N., Maternal serum interleukin-6 concentration as a marker for impending preterm delivery. Obstet. Gynecol. 91 (1998), 161–164.
11. Han, Y.W., Can oral bacteria cause pregnancy complications?. Women's Health 7 (2011), 401–404.
12. Han, Y.W., Oral health and adverse pregnancy outcomes - what's next?. J. Dent. Res. 90 (2011), 289–293.
13. Han, Y.W., Wang, X., Mobile microbiome: oral bacteria in extra-oral infections and inflammation. J. Dent. Res. 92 (2013), 485–491.
14. Barak, S., Oettinger-Barak, O., Oettinger, M., Machtei, E.E., Peled, M., Ohel, G., Common oral manifestations during pregnancy: a review. Obstet. Gynecol. Surv. 58 (2003), 624–628.
15. Jeffcoat, M.K., Geurs, N.C., Reddy, M.S., Cliver, S.P., Goldenberg, R.L., Hauth, J.C., Periodontal infection and preterm birth: results of a prospective study. J. Am. Dent. Assoc. 132 (2001), 875–880.
16. Jarjoura, K., Devine, P.C., Perez-Delboy, A., Herrera-Abreu, M., D'Alton, M., Papapanou, P.N., Markers of periodontal infection and preterm birth. Am. J. Obstet. Gynecol. 192 (2005), 513–519.
17. Turton, M., Africa, C.W., Further evidence for periodontal disease as a risk indicator for adverse pregnancy outcomes. Int. Dent. J. 67 (2017), 148–156.
18. Prince, A.L., Ma, J., Kannan, P.S., Alvarez, M., Gisslen, T., Harris, R.A., et al. The placental membrane microbiome is altered among subjects with spontaneous preterm birth with and without chorioamnionitis. Am. J. Obstet. Gynecol., 214, 2016, 627 e1- e16.
19. Amarasekara, R., Jayasekara, R.W., Senanayake, H., Dissanayake, V.H., Microbiome of the placenta in pre-eclampsia supports the role of bacteria in the multifactorial cause of pre-eclampsia. J. Obstet. Gynaecol. Res. 41 (2015), 662–669.
20. Pelzer, E., Gomez-Arango, L.F., Barrett, H.L., Nitert, M.D., Review: maternal health and the placental microbiome. Placenta 54 (2017), 30–37.
21. Lauder, A.P., Roche, A.M., Sherrill-Mix, S., Bailey, A., Laughlin, A.L., Bittinger, K., et al. Comparison of placenta samples with contamination controls does not provide evidence for a distinct placenta microbiota. Microbiome, 4, 2016, 29.
22. Aagaard, K., Ma, J., Antony, K.M., Ganu, R., Petrosino, J., Versalovic, J., The placenta harbors a unique microbiome. Sci. Transl. Med., 6, 2014, 237ra65.
23. Han, Y.W., Fardini, Y., Chen, C., Iacampo, K.G., Peraino, V.A., Shamonki, J.M., et al. Term stillbirth caused by oral Fusobacterium nucleatum. Obstet. Gynecol. 115 (2010), 442–445.
24. Han, Y.W., Shen, T., Chung, P., Buhimschi, I.A., Buhimschi, C.S., Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J. Clin. Microbiol. 47 (2009), 38–47.
25. Bohrer, J.C., Kamemoto, L.E., Almeida, P.G., Ogasawara, K.K., Acute chorioamnionitis at term caused by the oral pathogen Fusobacterium nucleatum. Hawai‘i J. Med. Public Health 71 (2012), 280–281.
26. Wang, X., Buhimschi, C.S., Temoin, S., Bhandari, V., Han, Y.W., Buhimschi, I.A., Comparative microbial analysis of paired amniotic fluid and cord blood from pregnancies complicated by preterm birth and early-onset neonatal sepsis. PLoS One, 8, 2013, e56131.
27. Moore, W.E., Moore, L.V., The bacteria of periodontal diseases. Periodontol. 2000 5 (1994), 66–77.
28. Griffen, A.L., Beall, C.J., Campbell, J.H., Firestone, N.D., Kumar, P.S., Yang, Z.K., et al. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J. 6 (2012), 1176–1185.
29. Strauss, J., Kaplan, G.G., Beck, P.L., Rioux, K., Panaccione, R., Devinney, R., et al. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm. Bowel Dis. 17 (2011), 1971–1978.
30. Allen-Vercoe, E., Strauss, J., Chadee, K., Fusobacterium nucleatum: an emerging gut pathogen?. Gut Microb. 2 (2011), 294–298.
31. Han, Y.W., Fusobacterium nucleatum: a commensal-turned pathogen. Curr. Opin. Microbiol. 23 (2015), 141–147.
32. Wahbeh, C.J., Hill, G.B., Eden, R.D., Gall, S.A., Intra-amniotic bacterial colonization in premature labor. Am. J. Obstet. Gynecol. 148 (1984), 739–743.
33. Miller, J.M. Jr., Pupkin, M.J., Hill, G.B., Bacterial colonization of amniotic fluid from intact fetal membranes. Am. J. Obstet. Gynecol. 136 (1980), 796–804.
34. Chaim, W., Mazor, M., Intraamniotic infection with fusobacteria. Arch. Gynecol. Obstet. 251 (1992), 1–7.
35. Cahill, R.J., Tan, S., Dougan, G., O'Gaora, P., Pickard, D., Kennea, N., et al. Universal DNA primers amplify bacterial DNA from human fetal membranes and link Fusobacterium nucleatum with prolonged preterm membrane rupture. Mol. Hum. Reprod. 11 (2005), 761–766.
36. Gonzales-Marin, C., Spratt, D.A., Allaker, R.P., Maternal oral origin of Fusobacterium nucleatum in adverse pregnancy outcomes as determined using the 16S-23S rRNA gene intergenic transcribed spacer region. J. Med. Microbiol. 62 (2013), 133–144.
37. Doyle, R.M., Alber, D.G., Jones, H.E., Harris, K., Fitzgerald, F., Peebles, D., et al. Term and preterm labour are associated with distinct microbial community structures in placental membranes which are independent of mode of delivery. Placenta 35 (2014), 1099–1101.
38. Gonzales-Marin, C., Spratt, D.A., Millar, M.R., Simmonds, M., Kempley, S.T., Allaker, R.P., Levels of periodontal pathogens in neonatal gastric aspirates and possible maternal sites of origin. Mol Oral Microbiol 26 (2011), 277–290.
39. Hill, G.B., Preterm birth: associations with genital and possibly oral microflora. Ann. Periodontol. 3 (1998), 222–232.
40. Gauthier, S., Tetu, A., Himaya, E., Morand, M., Chandad, F., Rallu, F., et al. The origin of Fusobacterium nucleatum involved in intra-amniotic infection and preterm birth. J. Matern. Fetal Neonatal Med.: the official journal of the European Association of Perinatal Medicine, the Federation of Asia and Oceania Perinatal Societies, the International Society of Perinatal Obstet 24 (2011), 1329–1332.
41. Fardini, Y., Chung, P., Dumm, R., Joshi, N., Han, Y.W., Transmission of diverse oral bacteria to murine placenta: evidence for the oral microbiome as a potential source of intrauterine infection. Infect. Immun. 78 (2010), 1789–1796.
42. Insoft, R.M., Sola, A., Perinatally acquired Pseudomonas infection: a newly recognized maternal risk factor. Am. J. Perinatol. 12 (1995), 25–26.
43. Ebersole, J.L., Novak, M.J., Michalowicz, B.S., Hodges, J.S., Steffen, M.J., Ferguson, J.E., et al. Systemic immune responses in pregnancy and periodontitis: relationship to pregnancy outcomes in the Obstetrics and Periodontal Therapy (OPT) study. J. Periodontol. 80 (2009), 953–960.
44. Hayman, L., Steffen, M.J., Stevens, J., Badger, E., Tempro, P., Fuller, B., et al. Smoking and periodontal disease: discrimination of antibody responses to pathogenic and commensal oral bacteria. Clin. Exp. Immunol. 164 (2011), 118–126.
45. Barak, S., Oettinger-Barak, O., Machtei, E.E., Sprecher, H., Ohel, G., Evidence of periopathogenic microorganisms in placentas of women with preeclampsia. J. Periodontol. 78 (2007), 670–676.
46. Swati, P., Thomas, B., Vahab, S.A., Kapaettu, S., Kushtagi, P., Simultaneous detection of periodontal pathogens in subgingival plaque and placenta of women with hypertension in pregnancy. Arch. Gynecol. Obstet. 285 (2012), 613–619.
47. Chaparro, A., Blanlot, C., Ramirez, V., Sanz, A., Quintero, A., Inostroza, C., et al. Porphyromonas gingivalis, Treponema denticola and toll-like receptor 2 are associated with hypertensive disorders in placental tissue: a case-control study. J. Periodontal. Res. 48 (2013), 802–809.
48. Holmlund, U., Cebers, G., Dahlfors, A.R., Sandstedt, B., Bremme, K., Ekstrom, E.S., et al. Expression and regulation of the pattern recognition receptors Toll-like receptor-2 and Toll-like receptor-4 in the human placenta. Immunology 107 (2002), 145–151.
49. Han, Y.W., Redline, R.W., Li, M., Yin, L., Hill, G.B., McCormick, T.S., Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect. Immun. 72 (2004), 2272–2279.
50. Liu, H., Redline, R.W., Han, Y.W., Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J. Immunol. 179 (2007), 2501–2508.
51. Kaplan, A., Kaplan, C.W., He, X., McHardy, I., Shi, W., Lux, R., Characterization of aid1, a novel gene involved in Fusobacterium nucleatum interspecies interactions. Microb. Ecol. 68 (2014), 379–387.
52. Kaplan, C.W., Lux, R., Haake, S.K., Shi, W., The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Mol. Microbiol. 71 (2009), 35–47.
53. Coppenhagen-Glazer, S., Sol, A., Abed, J., Naor, R., Zhang, X., Han, Y.W., et al. Fap2 of Fusobacterium nucleatum is a galactose-inhibitable adhesin involved in coaggregation, cell adhesion, and preterm birth. Infect. Immun. 83 (2015), 1104–1113.
54. Han, Y.W., Ikegami, A., Rajanna, C., Kawsar, H.I., Zhou, Y., Li, M., et al. Identification and characterization of a novel adhesin unique to oral fusobacteria. J. Bacteriol. 187 (2005), 5330–5340.
55. Xu, M., Yamada, M., Li, M., Liu, H., Chen, S.G., Han, Y.W., FadA from Fusobacterium nucleatum utilizes both secreted and nonsecreted forms for functional oligomerization for attachment and invasion of host cells. J. Biol. Chem. 282 (2007), 25000–25009.
56. Han, Y.W., Shi, W., Huang, G.T., Kinder Haake, S., Park, N.H., Kuramitsu, H., et al. Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells. Infect. Immun. 68 (2000), 3140–3146.
57. Nithianantham, S., Xu, M., Yamada, M., Ikegami, A., Shoham, M., Han, Y.W., Crystal structure of FadA adhesin from Fusobacterium nucleatum reveals a novel oligomerization motif, the leucine chain. J. Biol. Chem. 284 (2009), 3865–3872.
58. Ikegami, A., Chung, P., Han, Y.W., Complementation of the fadA mutation in Fusobacterium nucleatum demonstrates that the surface-exposed adhesin promotes cellular invasion and placental colonization. Infect. Immun. 77 (2009), 3075–3079.
59. Fardini, Y., Wang, X., Temoin, S., Nithianantham, S., Lee, D., Shoham, M., et al. Fusobacterium nucleatum adhesin FadA binds vascular endothelial cadherin and alters endothelial integrity. Mol. Microbiol. 82 (2011), 1468–1480.
60. Rubinstein, M.R., Wang, X., Liu, W., Hao, Y., Cai, G., Han, Y.W., Fusobacterium nucleatum promotes colorectal carcinogenesis by modulating E-cadherin/β-catenin signaling via its FadA adhesin. Cell Host Microbe 14 (2013), 195–206.