Skip to main content

Advertisement

SpringerLink
Log in

Increased periodontal inflammation in women with preterm premature rupture of membranes

  • Original Article
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objectives

To evaluate possible differences in periodontal inflammatory, microbiological and clinical parameters between women with preterm premature rupture of membranes (PPROM) and controls with uncomplicated pregnancies.

Materials and methods

Fifty-six women (32 test (PPROM) and 24 controls (uncomplicated pregnancies)) were examined at three time-points (T1: gestational weeks 20–35, T2: within 48 h after parturition, T3: 4–6 weeks after parturition). The examinations included assessment of the Periodontal Screening Index, collection of gingival crevicular fluid (GCF) and subgingival as well as vaginal bacterial sampling.

Results

Periodontal inflammation was found to be higher in the test compared with the control group (p < 0.05) and decreased over time in both groups (p < 0.05). Microbiological outcomes showed no intergroup differences (p > 0.05) in prevalence of bacteria, but a decrease in subgingival periodontopathogens from T1 to T2 in the test group (p < 0.05) was observed. Interleukin (IL)-1β levels in GCF at T2 were not different between groups (p > 0.05). In women with PPROM, GCF levels of IL-8 (p < 0.05) and C-reactive protein (p < 0.05) were lower and IL-10 levels higher (p < 0.05) compared with controls.

Conclusions

Periodontal inflammation is elevated during pregnancy and seems to be more pronounced in women with PPROM.

Clinical relevance

The findings of the present study revealed an association between periodontal inflammation and PPROM, thus emphasizing the importance of optimizing self-performed oral hygiene in pregnant women.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Beck S, Wojdyla D, Say L, Betran AP, Merialdi M, Requejo JH, Rubens C, Menon R, Van Look PF (2010) The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity. Bull World Health Organ 88(1):31–38

    Article  PubMed Central  PubMed  Google Scholar 

  2. Hamilton BE, Martin JA, Ventura SJ (2013) Births: preliminary data for 2012. Natl Vital Stat Rep 62(3):1–20

    Google Scholar 

  3. Bundesamt für Statistik (2012) Gesundheit der Neugeborenen. http://www.bfs.admin.ch/bfs/portal/de/index/themen/14/02/03/key/04.html

  4. Smith GC, Fretts RC (2007) Stillbirth. Lancet 370(9600):1715–1725

    Article  PubMed  Google Scholar 

  5. Lawn JE, Cousens S, Zupan J (2005) 4 million neonatal deaths: when? Where? Why. Lancet 365(9462):891–900

    Article  PubMed  Google Scholar 

  6. Callaghan WM, MacDorman MF, Rasmussen SA, Qin C, Lackritz EM (2006) The contribution of preterm birth to infant mortality rates in the United States. Pediatrics 118(4):1566–1573

    Article  PubMed  Google Scholar 

  7. Goldenberg RL, Culhane JF, Iams JD, Romero R (2008) Epidemiology and causes of preterm birth. Lancet 371(9606):75–84

    Article  PubMed  Google Scholar 

  8. Tucker JM, Goldenberg RL, Davis RO, Copper RL, Winkler CL, Hauth JC (1991) Etiologies of preterm birth in an indigent population: is prevention a logical expectation. Obstet Gynecol 77(3):343–347

    PubMed  Google Scholar 

  9. Mercer BM (2003) Preterm premature rupture of the membranes. Obstet Gynecol 101(1):178–193

    Article  PubMed  Google Scholar 

  10. Collins JG, Windley HW 3rd, Arnold RR, Offenbacher S (1994) Effects of a Porphyromonas gingivalis infection on inflammatory mediator response and pregnancy outcome in hamsters. Infect Immun 62(10):4356–4361

    PubMed Central  PubMed  Google Scholar 

  11. Chambrone L, Guglielmetti MR, Pannuti CM, Chambrone LA (2011) Evidence grade associating periodontitis to preterm birth and/or low birth weight: I. A systematic review of prospective cohort studies. J Clin Periodontol 38(9):795–808

    Article  PubMed  Google Scholar 

  12. Ide M, Papapanou PN (2013) Epidemiology of association between maternal periodontal disease and adverse pregnancy outcomes—systematic review. J Periodontol 84(4 Suppl):S181–S194

    PubMed  Google Scholar 

  13. Chambrone L, Pannuti CM, Guglielmetti MR, Chambrone LA (2011) Evidence grade associating periodontitis with preterm birth and/or low birth weight: II: a systematic review of randomized trials evaluating the effects of periodontal treatment. J Clin Periodontol 38(10):902–914

    Article  PubMed  Google Scholar 

  14. Weidlich P, Moreira CH, Fiorini T, Musskopf ML, da Rocha JM, Oppermann ML, Aass AM, Gjermo P, Susin C, Rosing CK, Oppermann RV (2013) Effect of nonsurgical periodontal therapy and strict plaque control on preterm/low birth weight: a randomized controlled clinical trial. Clin Oral Investig 17(1):37–44

    Article  PubMed  Google Scholar 

  15. Offenbacher S, Jared HL, O’Reilly PG, Wells SR, Salvi GE, Lawrence HP, Socransky SS, Beck JD (1998) Potential pathogenic mechanisms of periodontitis associated pregnancy complications. Ann Periodontol 3(1):233–250

    Article  PubMed  Google Scholar 

  16. Mitchell-Lewis D, Engebretson SP, Chen J, Lamster IB, Papapanou PN (2001) Periodontal infections and pre-term birth: early findings from a cohort of young minority women in New York. Eur J Oral Sci 109(1):34–39

    Article  PubMed  Google Scholar 

  17. Lin D, Moss K, Beck JD, Hefti A, Offenbacher S (2007) Persistently high levels of periodontal pathogens associated with preterm pregnancy outcome. J Periodontol 78(5):833–841

    Article  PubMed  Google Scholar 

  18. Madianos PN, Lieff S, Murtha AP, Boggess KA, Auten RL Jr, Beck JD, Offenbacher S (2001) Maternal periodontitis and prematurity. Part II: maternal infection and fetal exposure. Ann Periodontol 6(1):175–182

    Article  PubMed  Google Scholar 

  19. Noack B, Klingenberg J, Weigelt J, Hoffmann T (2005) Periodontal status and preterm low birth weight: a case control study. J Periodontal Res 40(4):339–345

    Article  PubMed  Google Scholar 

  20. Africa CWJ, Kayitenkore J, Bayingana C (2010) Examination of maternal gingival crevicular fluid for the presence of selected periodontopathogens implicated in the pre-term delivery of low birth weight infants. Virulence 1(4):254–259

    Article  PubMed  Google Scholar 

  21. Konopka T, Rutkowska M, Hirnle L, Kopec W, Karolewska E (2003) The secretion of prostaglandin E2 and interleukin 1-beta in women with periodontal diseases and preterm low-birth-weight. Bull Group Int Rech Sci Stomatol Odontol 45(1):18–28

    PubMed  Google Scholar 

  22. Carta G, Persia G, Falciglia K, Iovenitti P (2004) Periodontal disease and poor obstetrical outcome. Clin Exp Obstet Gynecol 31(1):47–49

    PubMed  Google Scholar 

  23. Tarannum F, Faizuddin M, Madaiah H (2011) Gingival crevicular fluid prostaglandin E2 level as a predictor of preterm low birth weight: a pilot investigation. J Oral Sci 53(3):293–300

    Article  PubMed  Google Scholar 

  24. Stadelmann P, Alessandri R, Eick S, Salvi GE, Surbek D, Sculean A (2013) The potential association between gingival crevicular fluid inflammatory mediators and adverse pregnancy outcomes: a systematic review. Clin Oral Investig 17(6):1453–1463

    Article  PubMed  Google Scholar 

  25. Abati S, Villa A, Cetin I, Dessole S, Luglie PF, Strohmenger L, Ottolenghi L, Campus GG (2013) Lack of association between maternal periodontal status and adverse pregnancy outcomes: a multicentric epidemiologic study. J Matern Fetal Neonatal 26(4):369–372

    Article  Google Scholar 

  26. Nabet C, Lelong N, Colombier ML, Sixou M, Musset AM, Goffinet F, Kaminski M (2010) Maternal periodontitis and the causes of preterm birth: the case–control Epipap study. J Clin Periodontol 37(1):37–45

    Article  PubMed Central  PubMed  Google Scholar 

  27. Radnai M, Gorzo I, Nagy E, Urban E, Eller J, Novak T, Pal A (2005) Caries and periodontal state of pregnant women. Part II periodontal state. Fogorv Sz 98(3):101–106

    PubMed  Google Scholar 

  28. Yang JL, Wang MS, Cheng AC, Pan KC, Li CF, Deng SX (2008) A simple and rapid method for extracting bacterial DNA from intestinal microflora for ERIC-PCR detection. World J Gastroenterol 14(18):2872–2876

    Article  PubMed Central  PubMed  Google Scholar 

  29. Jentsch H, Cachovan G, Guentsch A, Eickholz P, Pfister W, Eick S (2012) Characterization of Aggregatibacter actinomycetemcomitans strains in periodontitis patients in Germany. Clin Oral Investig 16(6):1589–1597

    Article  PubMed  Google Scholar 

  30. Canakci V, Canakci CF, Yildirim A, Ingec M, Eltas A, Erturk A (2007) Periodontal disease increases the risk of severe pre-eclampsia among pregnant women. J Clin Periodontol 34(8):639–645

    Article  PubMed  Google Scholar 

  31. Loe H, Silness J (1963) Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand 21:533–551

    Article  PubMed  Google Scholar 

  32. Kornman KS, Loesche WJ (1980) The subgingival microbial flora during pregnancy. J Periodontal Res 15(2):111–122

    Article  PubMed  Google Scholar 

  33. Figuero E, Carrillo-de-Albornoz A, Martin C, Tobias A, Herrera D (2013) Effect of pregnancy on gingival inflammation in systemically healthy women: a systematic review. J Clin Periodontol 40(5):457–473

    Article  PubMed  Google Scholar 

  34. Gursoy M, Pajukanta R, Sorsa T, Kononen E (2008) Clinical changes in periodontium during pregnancy and post-partum. J Clin Periodontol 35(7):576–583

    Article  PubMed  Google Scholar 

  35. Lieff S, Boggess KA, Murtha AP, Jared H, Madianos PN, Moss K, Beck J, Offenbacher S (2004) The oral conditions and pregnancy study: periodontal status of a cohort of pregnant women. J Periodontol 75(1):116–126

    Article  PubMed  Google Scholar 

  36. Adriaens LM, Alessandri R, Sporri S, Lang NP, Persson GR (2009) Does pregnancy have an impact on the subgingival microbiota. J Periodontol 80(1):72–81

    Article  PubMed  Google Scholar 

  37. Bieri RA, Adriaens L, Sporri S, Lang NP, Persson GR (2013) Gingival fluid cytokine expression and subgingival bacterial counts during pregnancy and postpartum: a case series. Clin Oral Investig 17(1):19–28

    Article  PubMed  Google Scholar 

  38. Lindhe J, Attsfrom R (1967) Gingival exudation during the menstrual cycle. J Periodontal Res 2(3):194–198

    Article  PubMed  Google Scholar 

  39. O’Neil TC (1979) Maternal T-lymphocyte response and gingivitis in pregnancy. J Periodontol 50(4):178–184

    Article  PubMed  Google Scholar 

  40. Carrillo-de-Albornoz A, Figuero E, Herrera D, Bascones-Martinez A (2010) Gingival changes during pregnancy: II. Influence of hormonal xvariations on the subgingival biofilm. J Clin Periodontol 37(3):230–240

    Article  PubMed  Google Scholar 

  41. Mariotti A (1994) Sex steroid hormones and cell dynamics in the periodontium. Crit Rev Oral Biol Med 5(1):27–53

    PubMed  Google Scholar 

  42. Kornman KS, Loesche WJ (1982) Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect Immun 35(1):256–263

    PubMed Central  PubMed  Google Scholar 

  43. Tsai CC, Chen KS (1995) A study on sex hormones in gingival crevicular fluid and black pigmented bacteria in subgingival plaque of pregnant women. Gaoxiong Yi Xue Ke Xue Za Zhi 11(5):265–273

    PubMed  Google Scholar 

  44. Yokoyama M, Hinode D, Yoshioka M, Fukui M, Tanabe S, Grenier D, Ito HO (2008) Relationship between Campylobacter rectus and periodontal status during pregnancy. Oral Microbiol Immunol 23(1):55–59

    Article  PubMed  Google Scholar 

  45. Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J (2014) The placenta harbors a unique microbiome. Sci Transl Med 6(237):237–265

    Article  Google Scholar 

  46. Oettinger-Barak O, Barak S, Ohel G, Oettinger M, Kreutzer H, Peled M, Machtei EE (2005) Severe pregnancy complication (preeclampsia) is associated with greater periodontal destruction. J Periodontol 76(1):134–137

    Article  PubMed  Google Scholar 

  47. Chaparro A, Sanz A, Quintero A, Inostroza C, Ramirez V, Carrion F, Figueroa F, Serra R, Illanes SE (2013) Increased inflammatory biomarkers in early pregnancy is associated with the development of pre-eclampsia in patients with periodontitis: a case control study. J Periodontal Res 48(3):302–307

    Article  PubMed  Google Scholar 

  48. Sato TA, Keelan JA, Mitchell MD (2003) Critical paracrine interactions between TNF-alpha and IL-10 regulate lipopolysaccharide-stimulated human choriodecidual cytokine and prostaglandin E2 production. J Immunol 170(1):158–166

    Article  PubMed  Google Scholar 

  49. Fortunato SJ, Menon R, Lombardi SJ (1998) The effect of transforming growth factor and interleukin-10 on interleukin-8 release by human amniochorion may regulate histologic chorioamnionitis. Am J Obstet Gynecol 179(3 Pt 1):794–799

    Article  PubMed  Google Scholar 

  50. Gotsch F, Romero R, Kusanovic JP, Erez O, Espinoza J, Kim CJ, Vaisbuch E, Than NG, Mazaki-Tovi S, Chaiworapongsa T, Mazor M, Yoon BH, Edwin S, Gomez R, Mittal P, Hassan SS, Sharma S (2008) The anti-inflammatory limb of the immune response in preterm labor, intra-amniotic infection/inflammation, and spontaneous parturition at term: a role for interleukin-10. J Matern Fetal Neonatal 21(8):529–547

    Article  Google Scholar 

  51. Cobo T, Kacerovsky M, Holst RM, Hougaard DM, Skogstrand K, Wennerholm UB, Hagberg H, Jacobsson B (2012) Intra-amniotic inflammation predicts microbial invasion of the amniotic cavity but not spontaneous preterm delivery in preterm prelabor membrane rupture. Acta Obstet Gynecol Scand 91(8):930–935

    Article  PubMed  Google Scholar 

  52. Cobo T, Kacerovsky M, Palacio M, Hornychova H, Hougaard DM, Skogstrand K, Jacobsson B (2012) A prediction model of histological chorioamnionitis and funisitis in preterm prelabor rupture of membranes: analyses of multiple proteins in the amniotic fluid. J Matern Fetal Neonatal 25(10):1995–2001

    Article  Google Scholar 

  53. Tsiartas P, Holst RM, Wennerholm UB, Hagberg H, Hougaard DM, Skogstrand K, Pearce BD, Thorsen P, Kacerovsky M, Jacobsson B (2012) Prediction of spontaneous preterm delivery in women with threatened preterm labour: a prospective cohort study of multiple proteins in maternal serum. BJOG 119(7):866–873

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors wish to acknowledge Professor Rutger Persson for his useful advices during initiation of this study and to express their appreciation for the laboratory work of Stéphanie Larti, Anna Magdon and Marianne Weibel. They are also grateful to the Department of Obstetrics and Gynecology, University Hospital Bern, the midwives and doctors and the women having participated in this study.

Source of funding and conflict of interest

This study has been funded by a grant from the Walter Haefner Stiftung, by the Clinical research fund of the Department of Obstetrics and Gynecology, University Hospital Bern and University of Bern, and by the Department of Periodontology, School of Dental Medicine, University of Bern. The authors report no conflicts of interest related to this study.

Author information

Authors and Affiliations

  1. Department of Periodontology, School of Dental Medicine, University of Bern, Freiburgstrasse 7, 3010, Bern, Switzerland

    Pascale F. M. Stadelmann, Sigrun Eick, Giovanni E. Salvi, Walter Bürgin, Christoph A. Ramseier & Anton Sculean

  2. Department of Obstetrics and Gynecology, University Hospital Bern and University of Bern, Bern, Switzerland

    Daniel Surbek & Stefan Mohr

Authors
  1. Pascale F. M. Stadelmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sigrun Eick
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Giovanni E. Salvi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel Surbek
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Stefan Mohr
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Walter Bürgin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Christoph A. Ramseier
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anton Sculean
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anton Sculean.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stadelmann, P.F.M., Eick, S., Salvi, G.E. et al. Increased periodontal inflammation in women with preterm premature rupture of membranes. Clin Oral Invest 19, 1537–1546 (2015). https://doi.org/10.1007/s00784-014-1371-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-014-1371-6

Keywords

Search

Navigation