The DOI matches its Crossref record; 52 of the 52 references it cites were found in a registry or an index.
Bacteria and Inflammatory Cells in Fetal Membranes Do Not Always Cause Preterm Labor
Open accessAbstract
Intrauterine infection has been frequently linked with preterm labor before 30 wk of human pregnancy. Many different species of organisms have been detected, leading to the suggestion that infection-induced preterm labor is a generic inflammatory response to organisms rather than a specific response to a limited number of pathogens. The detection of organisms by microbiological culture is a laborious and unreliable process, so the aim of this study was to harness modern molecular techniques to detect organisms in tissues from human pregnancy. A DNA probe specific for conserved regions of bacterial 16S ribosomal RNA sequence was designed and labeled with fluorescein for fluorescence in situ hybridization. Organisms were detected in the great majority (>80%) of fetal membranes after prolonged premature rupture of the fetal membranes and after preterm labor, which was consistent with previous data. Organisms were also detected in fetal membranes after preterm delivery without labor and in term deliveries (with or without labour). Inflammatory cells were found frequently in the amnion or chorion of preterm fetal membranes but not in term tissues. Our primary finding is that fluorescence in situ hybridization is an appropriate method to detect organisms in human fetal membranes. In addition, our data show that bacteria may be present in fetal membranes without necessarily causing an inflammatory response, so the mere presence of bacteria may not be sufficient to cause preterm labor.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The cited source says what the claim attributes to it.
In the citing paper
“Fluorescence in-situ hybridisation with a DNA probe specific for conserved regions of bacterial DNA (the 16S ribosomal RNA) has detected bacteria in the membranes of up to 70% of women undergoing elective caesarean section at term.85”
From Epidemiology and causes of preterm birth (2008) · cites this paper as [85]
The cited source says what the claim attributes to it.
In the citing paper
“These findings suggest that the presence of bacteria in the chorioamnion alone cannot be sufficient to cause an inflammatory response, preterm labour, and preterm birth.85”
From Epidemiology and causes of preterm birth (2008) · cites this paper as [85]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,253
Preeclampsia: An excessive maternal inflammatory response to pregnancy
Redman, C. W. G., Sacks, G. P., & Sargent, I. L. (1999) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(99)70239-5 · Cited by 1,838
A placental clock controlling the length of human pregnancy
McLean, M. P., Bisits, A. M., Davies, J., Woods, R., Lowry, P., & Smith, R. (1995) · Nature Medicine · doi:10.1038/nm0595-460 · Cited by 907
Sacks, G. P., Studená, K., Sargent, I. L., & Redman, C. W. G. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70254-6 · Cited by 823
Osman, I. (2003) · Molecular Human Reproduction · doi:10.1093/molehr/gag001 · Cited by 717
Romero, R., Sirtori, M., Oyarzun, E., Avila, C., Mazor, M., Callahan, R., Sabo, V., Athanassiadis, A. P., & Hobbins, J. C. (1989) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(89)90409-2 · Cited by 678
Greisen, K. S., Loeffelholz, M. J., Purohit, A. P., & Leong, D. (1994) · Journal of Clinical Microbiology · doi:10.1128/jcm.32.2.335-351.1994 · Cited by 626
Hillier, S. L., Witkin, S. S., Krohn, M. A., Watts, D. H., Kiviat, N. B., & Eschenbach, D. A. (1993) · PubMed · Cited by 581
Quantitative Bacteriology of Amniotic Fluid from Women with Clinical Intraamniotic Infection at Term
Gibbs, R. S., Blanco, J., Clair, P. J. S., & Castañeda, Y. S. (1982) · The Journal of Infectious Diseases · doi:10.1093/infdis/145.1.1 · Cited by 552
The preterm prediction study: significance of vaginal infections
Meis, P. J., Goldenberg, R. L., Mercer, B., Moawad, A., Das, A., McNellis, D., Johnson, F., Iams, J. D., Thom, E., & Andrews, W. W. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)91360-2 · Cited by 410
McGregor, J., French, J. I., Parker, R., Draper, D. L., Patterson, E., Jones, W., Thorsgard, K., & McFEE, J. G. (1995) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(95)90184-1 · Cited by 370
Schultsz, C., van den Berg, F. M., ten Kate, F. J. W., Tytgat, G. N. J., & Dankert, J. (1999) · Gastroenterology · doi:10.1016/s0016-5085(99)70393-8 · Cited by 311
King, A., Balendran, N., Wooding, P., Carter, N. P., & Loke, Y. W. (1990) · Journal of Immunology Research · doi:10.1155/1991/83493 · Cited by 277
Sobel, J. D. (2000) · Annual Review of Medicine · doi:10.1146/annurev.med.51.1.349 · Cited by 245
Campbell, S., Swann, H. R., Seif, M. W., Kimber, S. J., & Aplin, J. (1995) · Human Reproduction · doi:10.1093/humrep/10.6.1571 · Cited by 242
Prematurity: infection as an etiologic factor.
MINKOFF, H. L. (1983) · PubMed · Cited by 197
Vince, G. S., Starkey, P. M., Jackson, M. C., Sargent, I. L., & Redman, C. W. G. (1990) · Journal of Immunological Methods · doi:10.1016/0022-1759(90)90028-t · Cited by 178
Mechanism of Parturition and Preterm Labor
Challis, J. R. G. (2000) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-200010000-00025 · Cited by 172
KELLY, R. W. (1994) · Endocrine Reviews · doi:10.1210/edrv-15-5-684 · Cited by 169
Activation of Leukocytes During the Uteroplacental Passage in Preeclampsia
Mellembakken, J. R., Aukrust, P., Olafsen, M. K., Ueland, T., Hestdal, K., & Videm, V. (2002) · Hypertension · doi:10.1161/hy0102.100778 · Cited by 169
A longitudinal study of bacterial vaginosis during pregnancy
Hay, P., Morgan, D. J., ISON, C. A., Bhide, S. A., Romney, M. L., McKenzie, P., Pearson, J., Lamont, R., & TAYLOR‐ROBINSON, D. (1994) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1994.tb13580.x · Cited by 162
Challis, J. R. G., Lye, S. J., Gibb, W., Whittle, W. L., Patel, F. A., & Alfaidy, N. (2001) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2001.tb03804.x · Cited by 160
Placental microbiology and histology and the pathogenesis of chorioamnionitis.
Pankuch, G. A., Appelbaum, P. C., Lorenz, R. P., Botti, J. J., Schachter, J., & Naeye, R. L. (1984) · PubMed · Cited by 153
Romero, R. J., Mazor, M., Morrotti, R., Avila, C., Enrique Oyarzún, E., Insunza, A., Parra, M., Behnke, E., Montiel, F., & Cassell, G. H. (1992) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(92)91845-2 · Cited by 139
Burrows, T. D., King, A., & Loke, Y. W. (1994) · Placenta · doi:10.1016/s0143-4004(05)80233-4 · Cited by 128
Inflammatory mediators and parturition
KELLY, R. W. (1996) · Reviews of Reproduction · doi:10.1530/ror.0.0010089 · Cited by 125
Le-Barillec, K., Si‐Tahar, M., Balloy, V., & Chignard, M. (1999) · Journal of Clinical Investigation · doi:10.1172/jci5779 · Cited by 124
Burrows, T. D., King, A., & Loke, Y. W. (1994) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(94)90373-5 · Cited by 115
Maymon, E., Romero, R. J., Pacora, P., Gómez, R., Mazor, M., Edwin, S. S., Chaiworapongsa, T., Kim, J. C., Yoon, B. H., Menon, R., et al. (2001) · Journal of Perinatal Medicine · doi:10.1515/jpm.2001.044 · Cited by 115
Steinborn, A. (1996) · Obstetrics and Gynecology · doi:10.1016/0029-7844(96)00224-4 · Cited by 100
Licht, T. R., Krogfelt, K. A., Cohen, P. S., Poulsen, L. K., Urbance, J. W., & Molin, S. (1996) · Infection and Immunity · doi:10.1128/iai.64.9.3811-3817.1996 · Cited by 95
Krimmer, V., Merkert, H., von Eiff, C., Frosch, M., Eulert, J., Löhr, J. F., Hacker, J. H., & Ziebuhr, W. (1999) · Journal of Clinical Microbiology · doi:10.1128/jcm.37.8.2667-2673.1999 · Cited by 88
Bacterial vaginosis: Association with adverse pregnancy outcome
Kimberlin, D. F., & Andrews, W. W. (1998) · Seminars in Perinatology · doi:10.1016/s0146-0005(98)80012-8 · Cited by 85
A microbiologic and clinical study of placental inflammation at term
Dong, Y., Clair, P. J. S., & Ramzy, I. (1988) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(88)90371-2 · Cited by 79
Enrique Oyarzún, E., Masami Yamamoto, C., Katoa, S., Gómez, R., b, L. L., & Moenne, A. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70115-2 · Cited by 73
Histologic chorioamnionitis, microbial infection, and prematurity
Zlatnik, F. J., Gellhaus, T. M., Bénda, J., Koontz, F. P., & Burmeister, L. F. (1991) · International Journal of Gynecology & Obstetrics · doi:10.1016/0020-7292(91)90107-g · Cited by 59
Premature rupture of the membranes and ascending infection
Evaldson, G. R., Malmborg, A., & Nord, C. E. (1982) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1982.tb05028.x · Cited by 58
Gattone, V. H., MacNaughton, K. A., & Kraybill, A. L. (1996) · The Anatomical Record · doi:10.1002/(sici)1097-0185(199607)245:3 · Cited by 40
Evaluation of Amniotic Fluid for Aerobic and Anaerobic Bacteria
Lewis, J. F., Johnson, P., & Miller, P. H. (1976) · American Journal of Clinical Pathology · doi:10.1093/ajcp/65.1.58 · Cited by 39
Le-Barillec, K., Pidard, D., Balloy, V., & Chignard, M. (2000) · Journal of Leukocyte Biology · doi:10.1189/jlb.68.2.209 · Cited by 37
Characterization of Trophoblast Cell Isolations by a Modified Flow Cytometry Assay
Pötgens, A. J. G., Gaus, G., Frank, H., & Kaufmann, P. (2001) · Placenta · doi:10.1053/plac.2000.0597 · Cited by 31
Greig, P. C. (1998) · Clinical Obstetrics & Gynecology · doi:10.1097/00003081-199812000-00009 · Cited by 30
The biochemical role of platelet-activating factor in reproduction
Frenkel, R., Muguruma, K., & Johnston, J. M. (1996) · Progress in Lipid Research · doi:10.1016/0163-7827(96)00002-1 · Cited by 26
Kimber, S. J., Bentley, J., Ciemerych, M. A., Møller, C. J., & Bock, E. (1994) · PubMed · Cited by 23
Matsubara, S., Yamada, T., Minakami, H., Watanabe, T., Takizawa, T., & Sato, I. (1999) · Placenta · doi:10.1053/plac.1998.0366 · Cited by 23
Pröll, J., Blaschitz, A., Hartmann, M., Thalhamer, J., & Dohr, G. (1996) · PubMed · Cited by 21
Rapid and easy detection of Helicobacter pylori by in situ hybridization
Park, C.-S., & Kim, J. (1999) · Journal of Korean Medical Science · doi:10.3346/jkms.1999.14.1.15 · Cited by 18
The bacteriological environment of preterm infants.
Roos, P. J., Malan, A. F., Woods, D., Botha, P., Hyland, J., & Heese, H. D. V. (1980) · PubMed · Cited by 14
Adhesive Properties of Choriocarcinoma Cells toward Lymphocytes Activated or Not by Interleukin-2
Jarousseau, A.-C., Thibault, G., Reverdiau, P., Rodriguez, A., Lacord, M., de Russe, J., Watier, H., Degenne, D., Lebranchu, Y., Gruel, Y., et al. (1994) · Cellular Immunology · doi:10.1006/cimm.1994.1203 · Cited by 14
Mechanisms of Full-Term and Preterm Labor: Factors Influencing Uterine Activity
Ruiz, R. J. (1998) · Journal of Obstetric, Gynecologic & Neonatal Nursing · doi:10.1111/j.1552-6909.1998.tb02635.x · Cited by 6
Amniotic fluid infection at term.
Woods, D. L., Cc, S.-S., Malan, A. F., & Harrison, A. (1978) · PubMed · Cited by 4
Identification and in Situ Detection of Intracellular Bacteria in the Environment
Brand, B. C., Amann, R., Steinert, M., Grimm, D., & Hacker, J. H. (2000) · Sub-cellular biochemistry/Subcellular biochemistry · doi:10.1007/978-1-4757-4580-1_23 · Cited by 3
Research works printed but not linked: 9
- Minkoff H, 1983, Obstet Gynecol, 62, 137
- Hillier SL, 1993, Obstet Gynaecol, 81, 941
- Roos PJ, 1980, S Afr Med J, 57, 347
- Dong Y, 1987, Obstet Gynecol, 70, 175
- Woods DL, 1978, S Afr Med J, 53, 137
- Pankuch GA, 1984, Obstet Gynecol, 64, 802
- Zlatnik FJ, 1990, Obstet Gynecol, 76, 355
- Proll J, 1996, Early Pregnancy, 2, 271
- Kimber SJ, 1994, Eur J Cell Biol, 63, 102
Cited by
Sorted by citations
Epidemiology and causes of preterm birth
Goldenberg, R. L., Culhane, J. F., Iams, J. D., & Romero, R. (2008) · The Lancet · doi:10.1016/s0140-6736(08)60074-4 · Cited by 7,801
Milani, C., Duranti, S., Bottacini, F., Casey, E., Turroni, F., Mahony, J., Belzer, C., Delgado Palacio, S., Arboleya Montes, S., Mancabelli, L., et al. (2017) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00036-17 · Cited by 1,950
The preterm parturition syndrome
Romero, R., Espinoza, J., Kusanovic, J., Gotsch, F., Hassan, S., Erez, O., Chaiworapongsa, T., & Mazor, M. (2006) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.2006.01120.x · Cited by 1,419
The composition of the gut microbiota throughout life, with an emphasis on early life
Rodríguez, J. M., Murphy, K., Stanton, C., Ross, R. P., Kober, O. I., Juge, N., Avershina, E., Rudi, K., Narbad, A., Jenmalm, M. C., et al. (2015) · Microbial Ecology in Health and Disease · doi:10.3402/mehd.v26.26050 · Cited by 1,414
The microbiome in early life: Implications for health outcomes
Tamburini, S., Shen, N., Wu, H. C., & Clemente, J. C. (2016) · Nature Medicine · doi:10.1038/nm.4142 · Cited by 1,213
Metadata
- Authors
- Steel, J. H., Malatos, S., Kennea, N., Edwards, A. D., Miles, L., Duggan, P., Reynolds, P. R., Feldman, R. G., & Sullivan, M. H. F.
- Affiliations
- Imperial College London (GB)
- Hammersmith Hospital (GB)
- Corresponding author
- Sullivan, Mark H F
- Venue
- Pediatric Research
- Published
- 2005-03
- Volume
- 57
- Issue
- 3
- Pages
- 404-411
- ISSN
- 0031-3998 (ISSN-L)
- 1530-0447
- OpenAlex
- W2025568822
- Cited by
- 317
- References
- 52
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 11 · 2023: 16 · 2022: 11 · 2021: 26 · 2020: 28 · 2019: 16 · 2018: 23 · 2017: 35 · 2016: 23 · 2015: 19 · 2014: 21 · 2013: 9 · 2012: 13
- FWCI
- 6.00
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Pediatric Research (publishedVersion)
- PubMed (publishedVersion)
- Research Portal (King's College London) (publishedVersion, other-oa)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Preterm Birth and Chorioamnionitis
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Neonatal and Maternal Infections
- Life Sciences › Immunology and Microbiology › Microbiology › Reproductive tract infections research
- Keywords
- preterm labor, fetal membranes, intrauterine infection, bacterial 16S rRNA, fluorescence in situ hybridization, bacterial detection, inflammatory cells, amniotic membrane, chorion, premature rupture of membranes, preterm birth, term pregnancy
- MeSH terms
- Bacteria, Female, Extraembryonic Membranes, Fetal Membranes, Premature Rupture, Premature Rupture of Fetal Membranes, Gestational Age, Humans, Immune System, Obstetric Labor, Premature, Pregnancy, RNA, Bacterial, RNA, Ribosomal, 16S, Nucleic Acid Probes, Antigens, CD, In Situ Hybridization, In Situ Hybridization, Fluorescence, Premature Birth
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review