Maternal oral origin of fusobacterium nucleatum in adverse pregnancy outcomes as determined using the 16S-23S rRNA gene intergenic transcribed spacer region

Journal of Medical Microbiology

Volumn 62, Issue PART1, 2013, Pages 133-144

  Gonzales Marin, Cecilia ^a   Spratt, David A ^b   Allaker, Robert P ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

INTERNAL TRANSCRIBED SPACER; PRIMER RNA; RNA 16S; RNA 23S;

ADVERSE OUTCOME; AMNION FLUID; ARTICLE; BACTERIAL STRAIN; BACTERIUM IDENTIFICATION; CONTROLLED STUDY; FEMALE; FUSOBACTERIUM NUCLEATUM; GASTRIC SUCTION; GENE AMPLIFICATION; HUMAN; HUMAN TISSUE; MOLECULAR CLONING; NEWBORN INFECTION; NONHUMAN; OPERON; PERIODONTICS; POLYMERASE CHAIN REACTION; PREGNANCY OUTCOME; PREMATURITY; PRIORITY JOURNAL; RNA SEQUENCE; SUBSPECIES; VAGINA;

BASE SEQUENCE; CLONING, MOLECULAR; DNA, RIBOSOMAL SPACER; FEMALE; FUSOBACTERIUM INFECTIONS; FUSOBACTERIUM NUCLEATUM; HUMANS; INFANT, NEWBORN; MOLECULAR SEQUENCE DATA; MOUTH; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; RNA, RIBOSOMAL, 16S; RNA, RIBOSOMAL, 23S;

EID: 84871163920     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.049452-0     Document Type: Article

References (46)

1. Bearfield, C., Davenport, E. S., Sivapathasundaram, V. & Allaker, R. P. (2002). Possible association between amniotic fluid microorganism infection and microflora in the mouth. BJOG 109, 527-533.
2. Benson, D. A., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. (2011). GenBank. Nucleic Acids Res 39 (Database issue), D32-D37.
3. Berres, F., Resch, G., Ruppert, M., Meyer, J. & Kulik, E. M. (2003). [Ribotyping Fusobacterium nucleatum isolates from healthy and diseased periodontium]. Schweiz Monatsschr Zahnmed 113, 953-957 (in German).
4. Bolstad, A. I., Jensen, H. B. & Bakken, V. (1996). Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clin Microbiol Rev 9, 55-71.
5. Chen, T., Yu, W. H., Izard, J., Baranova, O. V., Lakshmanan, A. & Dewhirst, F. E. (2010). The human oral microbiome database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) 2010, baq013.
6. Christensen, H., Jørgensen, K. & Olsen, J. E. (1999). Differentiation of Campylobacter coli and C. jejuni by length and DNA sequence of the 16S-23S rRNA internal spacer region. Microbiology 145, 99-105.
7. Cole, J. R., Chai, B., Farris, R. J., Wang, Q., Kulam-Syed-Mohideen, A. S., McGarrell, D. M., Bandela, A. M., Cardenas, E., Garrity, G. M. & Tiedje, J. M. (2007). The ribosomal database project (RDP-II): introducing myRDP space and quality controlled public data. Nucleic Acids Res 35 (Database issue,), D169-D172.
8. Conrads, G., Claros, M. C., Citron, D. M., Tyrrell, K. L., Merriam, V. & Goldstein, E. J. (2002). 16S-23S rDNA internal transcribed spacer sequences for analysis of the phylogenetic relationships among species of the genus Fusobacterium. Int J Syst Evol Microbiol 52, 493-499.
9. Corpet, F. (1988). Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16, 10881-10890.
10. Dewhirst, F. E., Chen, T., Izard, J., Paster, B. J., Tanner, A. C., Yu, W. H., Lakshmanan, A. & Wade, W. G. (2010). The human oral microbiome. J Bacteriol 192, 5002-5017.
11. Dzink, J. L., Sheenan, M. T. & Socransky, S. S. (1990). Proposal of three subspecies of Fusobacterium nucleatum Knorr 1922: Fusobacterium nucleatum subsp. nucleatum subsp. nov., comb. nov.; Fusobacterium nucleatum subsp. polymorphum subsp. nov., nom. rev., comb. nov.; and Fusobacterium nucleatum subsp. vincentii subsp. nov., nom. rev., comb. nov. Int J Syst Bacteriol 40, 74-78.
12. Gharbia, S. E. & Shah, H. N. (1992). Fusobacterium nucleatum subsp. fusiforme subsp. nov. and Fusobacterium nucleatum subsp. animalis subsp. nov. as additional subspecies within Fusobacterium nucleatum. Int J Syst Bacteriol 42, 296-298.
13. Gharbia, S. E., Shah, H. N., Lawson, P. A. & Haapasalo, M. (1990). Distribution and frequency of Fusobacterium nucleatum subspecies in the human oral cavity. Oral Microbiol Immunol 5, 324-327.
14. Gmür, R., Munson, M. A. & Wade, W. G. (2006). Genotypic and phenotypic characterization of fusobacteria from Chinese and European patients with inflammatory periodontal diseases. Syst Appl Microbiol 29, 120-130.
15. Goldstein, E. J., Summanen, P. H., Citron, D. M., Rosove, M. H. & Finegold, S. M. (1995). Fatal sepsis due to a b-lactamase-producing strain of Fusobacterium nucleatum subspecies polymorphum. Clin Infect Dis 20, 797-800.
16. Gonzales-Marin, C., Spratt, D. A., Millar, M. R., Simmonds, M., Kempley, S. T. & Allaker, R. P. (2011). Levels of periodontal pathogens in neonatal gastric aspirates and possible maternal sites of origin. Mol Oral Microbiol 26, 277-290.
17. Gonzales-Marin, C., Spratt, D. A., Millar, M. R., Simmonds, M., Kempley, S. T. & Allaker, R. P. (2012). Identification of bacteria and potential sources in neonates at risk of infection delivered by caesarean and vaginal birth. J Med Microbiol 61, 31-41.
18. Gürtler, V. & Stanisich, V. A. (1996). New approaches to typing and identification of bacteria using the 16S-23S rDNA spacer region. Microbiology 142, 3-16.
19. Han, Y. W., Shi, W., Huang, G. T., Kinder Haake, S., Park, N.-H., Kuramitsu, H. & Genco, R. J. (2000). Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells. Infect Immun 68, 3140-3146.
20. Han, Y. W., Redline, R. W., Li, M., Yin, L., Hill, G. B. & McCormick, T. S. (2004). Fusobacterium nucleatum induces premature and term stillbirths in pregnant mice: implication of oral bacteria in preterm birth. Infect Immun 72, 2272-2279.
21. Han, Y. W., Ikegami, A., Bissada, N. F., Herbst, M., Redline, R. W. & Ashmead, G. G. (2006). 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.
22. Han, Y. W., Shen, T., Chung, P., Buhimschi, I. A. & Buhimschi, C. S. (2009). Uncultivated bacteria as etiologic agents of intra-amniotic inflammation leading to preterm birth. J Clin Microbiol 47, 38-47.
23. Han, Y. W., Fardini, Y., Chen, C., Iacampo, K. G., Peraino, V. A., Shamonki, J. M. & Redline, R. W. (2010). Term stillbirth caused by oral Fusobacterium nucleatum. Obstet Gynecol 115 (Supplement,), 442-445.
24. Hill, G. B. (1998). Preterm birth: associations with genital and possibly oral microflora. Ann Periodontol 3, 222-232.
25. Ikegami, A., Chung, P. & Han, Y. W. (2009). Complementation of the fadA mutation in Fusobacterium nucleatum demonstrates that the surface-exposed adhesin promotes cellular invasion and placental colonization. Infect Immun 77, 3075-3079.
26. Jeffcoat, M., Parry, S., Sammel, M., Clothier, B., Catlin, A. & Macones, G. (2011). Periodontal infection and preterm birth: successful periodontal therapy reduces the risk of preterm birth. BJOG 118, 250-256.
27. Kapatral, V., Anderson, I., Ivanova, N., Reznik, G., Los, T., Lykidis, A., Bhattacharyya, A., Bartman, A., Gardner, W. & other authors (2002). Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J Bacteriol 184, 2005-2018.
28. Karpathy, S. E., Qin, X., Gioia, J., Jiang, H., Liu, Y., Petrosino, J. F., Yerrapragada, S., Fox, G. E., Haake, S. K. & other authors (2007). Genome sequence of Fusobacterium nucleatum subspecies polymorphum -a genetically tractable fusobacterium. PLoS ONE 2, e659.
29. Kim, H.-S., Lee, D.-S., Chang, Y.-H., Kim, M. J., Koh, S., Kim, J., Seong, J.-H., Song, S. K., Shin, H. S. &other authors (2010). Application of rpoB and zinc protease gene for use in molecular discrimination of Fusobacterium nucleatum subspecies. J Clin Microbiol 48, 545-553.
30. Lawson, P. A., Gharbia, S. E., Shah, H. N., Clark, D. R. & Collins, M. D. (1991). Intrageneric relationships of members of the genus Fusobacterium as determined by reverse transcriptase sequencing of small-subunit rRNA. Int J Syst Bacteriol 41, 347-354.
31. Liu, H., Redline, R. W. & Han, Y. W. (2007). Fusobacterium nucleatum induces fetal death in mice via stimulation of TLR4-mediated placental inflammatory response. J Immunol 179, 2501-2508.
32. Miralles, R., Hodge, R., McParland, P. C., Field, D. J., Bell, S. C., Taylor, D. J., Grant, W. D. & Kotecha, S. (2005). Relationship between antenatal inflammation and antenatal infection identified by detection of microbial genes by polymerase chain reaction. Pediatr Res 57, 570-577.
33. Nagano, Y., Watabe, M., Porter, K. G., Coulter, W. A., Millar, B. C., Elborn, J. S., Goldsmith, C. E., Rooney, P. J., Loughrey, A. & Moore, J. E. (2007). Development of a genus-specific PCR assay for the molecular detection, confirmation and identification of Fusobacterium spp. Br J Biomed Sci 64, 74-77.
34. Narayanan, S. K., Nagaraja, T. G., Chengappa, M. M. & Stewart, G. C. (2001). Electrophoretic mobility anomalies associated with PCR amplification of the intergenic spacer region between 16S and 23S ribosomal RNA genes of Fusobacterium necrophorum. J Microbiol Methods 46, 165-169.
35. Offenbacher, S., Katz, V., Fertik, G., Collins, J., Boyd, D., Maynor, G., McKaig, R. & Beck, J. (1996). Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 67 (Suppl), 1103-1113.
36. Paster, B. J., Boches, S. K., Galvin, J. L., Ericson, R. E., Lau, C. N., Levanos, V. A., Sahasrabudhe, A. & Dewhirst, F. E. (2001). Bacterial diversity in human subgingival plaque. J Bacteriol 183, 3770-3783.
37. Patel, J. B. (2001). 16S rRNA gene sequencing for bacterial pathogen identification in the clinical laboratory. Mol Diagn 6, 313-321.
38. Popa, R., Popa, R., Mashall, M. J., Nguyen, H., Tebo, B. M. & Brauer, S. (2009). Limitations and benefits of ARISA intra-genomic diversity fingerprinting. J Microbiol Methods 78, 111-118.
39. Sadeghifard, N., Gürtler, V., Beer, M. & Seviour, R. J. (2006). The mosaic nature of intergenic 16S-23S rRNA spacer regions suggests rRNA operon copy number variation in Clostridium difficile strains. Appl Environ Microbiol 72, 7311-7323.
40. Saito, A., Inagaki, S., Kimizuka, R., Okuda, K., Hosaka, Y., Nakagawa, T. & Ishihara, K. (2008). Fusobacterium nucleatum enhances invasion of human gingival epithelial and aortic endothelial cells by Porphyromonas gingivalis. FEMS Immunol Med Microbiol 54, 349-355.
41. Söller, R., Hirsch, P., Blohm, D. & Labrenz, M. (2000). Differentiation of newly described antarctic bacterial isolates related to Roseobacter species based on 16S-23S rDNA internal transcribed spacer sequences. Int J Syst Evol Microbiol 50, 909-915.
42. Strauss, J., White, A., Ambrose, C., McDonald, J. & Allen-Vercoe, E. (2008). Phenotypic and genotypic analyses of clinical Fusobacterium nucleatum and Fusobacterium periodonticum isolates from the human gut. Anaerobe 14, 301-309.
43. Tateishi, F., Hasegawa-Nakamura, K., Nakamura, T., Oogai, Y., Komatsuzawa, H., Kawamata, K., Douchi, T., Hatae, M. & Noguchi, K. (2012). Detection of Fusobacterium nucleatum in chorionic tissues of high-risk pregnant women. J Clin Periodontol 39, 417-424.
44. Tyrrell, G. J., Bethune, R. N., Willey, B. & Low, D. E. (1997). Species identification of enterococci via intergenic ribosomal PCR. J Clin Microbiol 35, 1054-1060.
45. Wang, G. C. & Wang, Y. (1997). Frequency of formation of chimeric molecules as a consequence of PCR coamplification of 16S rRNA genes from mixed bacterial genomes. Appl Environ Microbiol 63, 4645-4650.
46. Xie, H., Gibbons, R. J. & Hay, D. I. (1991). Adhesive properties of strains of Fusobacterium nucleatum of the subspecies nucleatum, vincentii and polymorphum. Oral Microbiol Immunol 6, 257-263.