Skip to main content

Advertisement

SpringerLink
Log in

Relationship between periodontal parameters and plasma cytokine profiles in pregnant woman with preterm birth or low birth weight

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

A Correction to this article was published on 03 September 2020

This article has been updated

Abstract

Objectives

The aim was to determine whether clinical periodontal parameters are associated with plasma anti- and/or pro-inflammatory cytokines in pregnant woman with preterm birth (PB) or low birth weight (LBW) neonates.

Materials and methods

An observational case-control study was performed in 131 puerperal women: mothers of PB/LBW neonates (cases, n = 67) and mothers of full-term normal-weight neonates (controls, n = 64). Sociodemographic and periodontal data was gathered from all participants, and interleukin (IL)-1β, IL-6, IL-8, IL-10, IL-17, IL-23, and tumor necrosis factor alpha (TNF-α) were determined in plasma.

Results

In multiple linear regression models, clinical attachment loss was associated with TNF-α (0.28 ± 0.14; 95 % confidence interval (CI) [0.006, 0.553]) and IL-1β (0.43 ± 0.21; 95 %CI [0.018, 0.842]), independent of group membership. IL-1β (−1.67 ± 0.27, 95 %CI [−2.199, −1.141]), IL-6 (−0.86 ± 0.27; 95 %CI [−1.389, −0.331]), and IL-8 (−3.84 ± 0.50, 95 %CI [−4.820, −2.860]) were lower, and IL-10 (0.86 ± 0.26; 95 %CI [0.350, 1.370]) was higher in cases versus controls after adjusting for potential confounders.

Conclusions

Clinical attachment loss was associated with plasma TNF-α and IL-1β levels. No plasma cytokine profiles suggestive of systemic inflammatory response were observed in the pregnant women with PB/LBW neonates.

Clinical relevance

Clinical attachment loss, as the main periodontal measure, is associated with TNF-α and IL-1β plasma levels in pregnant women. No relationship was found between PB/LBW and the markers of systemic inflammatory response assessed in this study.

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

Similar content being viewed by others

Change history

  • 03 September 2020

    The authors are correcting this article because they accidentally included some wrong data in the analysis.

References

  1. Chang HH, Larson J, Blencowe H, Spong CY, Howson CP, Cairns-Smith S, Lackritz EM, Lee SK, Mason E, Serazin AC, Walani S, Simpson JL, Lawn JE (2013) Preventing preterm births: analysis of trends and potential reductions with interventions in 39 countries with very high human development index. Lancet 381(9862):223–234. doi:10.1016/S0140-6736(12)61856-X

    Article  PubMed  PubMed Central  Google Scholar 

  2. Sanz M, Kornman K, Working group 3 of joint EFPAAPw (2013) Periodontitis and adverse pregnancy outcomes: consensus report of the Joint EFP/AAP Workshop on Periodontitis and Systemic Diseases. J Clin Periodontol 40(Suppl 14):S164–169. doi:10.1111/jcpe.12083

    PubMed  Google Scholar 

  3. 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. doi:10.1111/j.1600-051X.2011.01755.x

    Article  PubMed  Google Scholar 

  4. Wimmer G, Pihlstrom BL (2008) A critical assessment of adverse pregnancy outcome and periodontal disease. J Clin Periodontol 35(8 Suppl):380–397. doi:10.1111/j.1600-051X.2008.01284.x

    Article  PubMed  Google Scholar 

  5. Graves D (2008) Cytokines that promote periodontal tissue destruction. J Periodontol 79(8 Suppl):1585–1591. doi:10.1902/jop.2008.080183

    Article  PubMed  Google Scholar 

  6. Thunell DH, Tymkiw KD, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, Brogden KA, Guthmiller JM (2010) A multiplex immunoassay demonstrates reductions in gingival crevicular fluid cytokines following initial periodontal therapy. J Periodontal Res 45(1):148–152. doi:10.1111/j.1600-0765.2009.01204.x

    Article  PubMed  Google Scholar 

  7. Fiorini T, Vianna P, Weidlich P, Musskopf ML, Moreira CH, Chies JA, Rosing CK, Oppermann RV, Susin C (2012) Relationship between cytokine levels in serum and gingival crevicular fluid (GCF) in pregnant women. Cytokine 58(1):34–39. doi:10.1016/j.cyto.2011.12.015

    Article  PubMed  Google Scholar 

  8. Sert T, Kirzioglu FY, Fentoglu O, Aylak F, Mungan T (2011) Serum placental growth factor, vascular endothelial growth factor, soluble vascular endothelial growth factor receptor-1 and -2 levels in periodontal disease, and adverse pregnancy outcomes. J Periodontol 82(12):1735–1748. doi:10.1902/jop.2011.100740

    Article  PubMed  Google Scholar 

  9. Michalowicz BS, Novak MJ, Hodges JS, DiAngelis A, Buchanan W, Papapanou PN, Mitchell DA, Ferguson JE, Lupo V, Bofill J, Matseoane S, Steffen M, Ebersole JL (2009) Serum inflammatory mediators in pregnancy: changes after periodontal treatment and association with pregnancy outcomes. J Periodontol 80(11):1731–1741. doi:10.1902/jop.2009.090236

    Article  PubMed  PubMed Central  Google Scholar 

  10. Madianos PN, Bobetsis YA, Offenbacher S (2013) Adverse pregnancy outcomes (APOs) and periodontal disease: pathogenic mechanisms. J Clin Periodontol 40(Suppl 14):S170–S180. doi:10.1111/jcpe.12082

    PubMed  Google Scholar 

  11. Cohen J (1988) Statistical power analysis for the behavioural sciences. 2° Ed. edn. Lawrence Erlbaum Associates, New Jersey

  12. Regidor E, de Trabajo de la Grupo SEE (2001) The Goldthorpe Social Class Classification: reference framework for a proposal for the measurement of social class by the Working Group of the Spanish Society of Epidemiology. Rev Esp Salud Publica 75(1):13–22

    Article  PubMed  Google Scholar 

  13. Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33(1):159–174

    Article  PubMed  Google Scholar 

  14. Ainamo J, Bay I (1975) Problems and proposals for recording gingivitis and plaque. Int Dent J 25(4):229–235

    PubMed  Google Scholar 

  15. Lopez NJ, Smith PC, Gutierrez J (2002) Higher risk of preterm birth and low birth weight in women with periodontal disease. J Dent Res 81(1):58–63

    Article  PubMed  Google Scholar 

  16. Doménech Massons J, Sarriá Arrufat A (1993) Análisis multivariante en ciencias de la salud. Construcción de un modelo de regresión múltiple [In Spanish]. Editorial Gráficas SIGNO, Barcelona

  17. Szarka A, Rigo J Jr, Lazar L, Beko G, Molvarec A (2010) Circulating cytokines, chemokines and adhesion molecules in normal pregnancy and preeclampsia determined by multiplex suspension array. BMC Immunol 11:59. doi:10.1186/1471-2172-11-59

    Article  PubMed  PubMed Central  Google Scholar 

  18. Hasegawa-Nakamura K, Tateishi F, Nakamura T, Nakajima Y, Kawamata K, Douchi T, Hatae M, Noguchi K (2011) The possible mechanism of preterm birth associated with periodontopathic Porphyromonas gingivalis. J Periodontal Res 46(4):497–504. doi:10.1111/j.1600-0765.2011.01366.x

    Article  PubMed  Google Scholar 

  19. 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(5):417–424. doi:10.1111/j.1600-051X.2012.01855.x

    Article  PubMed  Google Scholar 

  20. Manau C, Echeverria A, Agueda A, Guerrero A, Echeverria JJ (2008) Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes. J Clin Periodontol 35(5):385–397. doi:10.1111/j.1600-051X.2008.01222.x

    Article  PubMed  Google Scholar 

  21. Guimaraes AN, Silva-Mato A, Miranda Cota LO, Siqueira FM, Costa FO (2010) Maternal periodontal disease and preterm or extreme preterm birth: an ordinal logistic regression analysis. J Periodontol 81(3):350–358. doi:10.1902/jop.2009.090527

    Article  PubMed  Google Scholar 

  22. Romero R, Baumann P, Gonzalez R, Gomez R, Rittenhouse L, Behnke E, Mitchell MD (1994) Amniotic fluid prostanoid concentrations increase early during the course of spontaneous labor at term. Am J Obstet Gynecol 171(6):1613–1620

    Article  PubMed  Google Scholar 

  23. Greig PC, Murtha AP, Jimmerson CJ, Herbert WN, Roitman-Johnson B, Allen J (1997) Maternal serum interleukin-6 during pregnancy and during term and preterm labor. Obstet Gynecol 90(3):465–469

    Article  PubMed  Google Scholar 

  24. Opsjln SL, Wathen NC, Tingulstad S, Wiedswang G, Sundan A, Waage A, Austgulen R (1993) Tumor necrosis factor, interleukin-1, and interleukin-6 in normal human pregnancy. Am J Obstet Gynecol 169(2 Pt 1):397–404

    Article  PubMed  Google Scholar 

  25. Wei SQ, Fraser W, Luo ZC (2010) Inflammatory cytokines and spontaneous preterm birth in asymptomatic women: a systematic review. Obstet Gynecol 116(2 Pt 1):393–401. doi:10.1097/AOG.0b013e3181e6dbc0

    Article  PubMed  Google Scholar 

  26. Perozini C, Chibebe PC, Leao MV, Queiroz Cda S, Pallos D (2010) Gingival crevicular fluid biochemical markers in periodontal disease: a cross-sectional study. Quintessence Int 41(10):877–883

    PubMed  Google Scholar 

  27. Santos VR, Ribeiro FV, Lima JA, Napimoga MH, Bastos MF, Duarte PM (2010) Cytokine levels in sites of chronic periodontitis of poorly controlled and well-controlled type 2 diabetic subjects. J Clin Periodontol 37(12):1049–1058. doi:10.1111/j.1600-051X.2010.01624.x

    Article  PubMed  Google Scholar 

  28. 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. doi:10.1902/annals.1998.3.1.233

    Article  PubMed  Google Scholar 

  29. 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. doi:10.1111/j.1600-051X.2007.01105.x

    Article  PubMed  Google Scholar 

  30. 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. doi:10.1007/s00784-013-0952-0

    Article  PubMed  Google Scholar 

  31. Lin D, Smith MA, Champagne C, Elter J, Beck J, Offenbacher S (2003) Porphyromonas gingivalis infection during pregnancy increases maternal tumor necrosis factor alpha, suppresses maternal interleukin-10, and enhances fetal growth restriction and resorption in mice. Infect Immun 71(9):5156–5162

    Article  PubMed  PubMed Central  Google Scholar 

  32. Noh MK, Jung M, Kim SH, Lee SR, Park KH, Kim DH, Kim HH, Park YG (2013) Assessment of IL-6, IL-8 and TNF-alpha levels in the gingival tissue of patients with periodontitis. Exp Ther Med 6(3):847–851. doi:10.3892/etm.2013.1222

    PubMed  PubMed Central  Google Scholar 

  33. Trinchieri G (2007) Interleukin-10 production by effector T cells: Th1 cells show self control. J Exp Med 204(2):239–243. doi:10.1084/jem.20070104

    Article  PubMed  PubMed Central  Google Scholar 

  34. Qi Y, Feng W, Song A, Song H, Yan S, Sun Q, Yang P (2013) Role of serum IL-23/IL-17 axis in the relationship between periodontitis and coronary heart disease. Int J Periodontics Restorative Dent 33 (2):185-191. doi:10.11607/prd.1327

  35. Ohyama H, Kato-Kogoe N, Kuhara A, Nishimura F, Nakasho K, Yamanegi K, Yamada N, Hata M, Yamane J, Terada N (2009) The involvement of IL-23 and the Th17 pathway in periodontitis. J Dent Res 88(7):633–638. doi:10.1177/0022034509339889

    Article  PubMed  Google Scholar 

Download references

Conflict of interest

The authors declare no financial interests, either directly or indirectly, in the products or information listed in the paper.

Author information

Authors and Affiliations

  1. Periodontology Department, School of Dentistry, University of Granada, Campus de Cartuja s/n, 18071, Granada, Spain

    Francisco Mesa, Elena Pozo & Antonio Magan-Fernandez

  2. Pathology Department, School of Medicine, University of Granada, Avda. De Madrid s/n, 18012, Granada, Spain

    Francisco O’Valle

  3. Department of Obstetrics and Gynecology, Virgen de las Nieves University Hospital, Avda. Fuerzas Armadas 2, 18014, Granada, Spain

    Alberto Puertas

  4. Department of Preventive Dentistry and Epidemiology, School of Dentistry, University of Granada, Campus de Cartuja s/n, 18071, Granada, Spain

    Eva Rosel & Manuel Bravo

Authors
  1. Francisco Mesa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elena Pozo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Francisco O’Valle
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Alberto Puertas
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Antonio Magan-Fernandez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Eva Rosel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Manuel Bravo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Francisco Mesa.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mesa, F., Pozo, E., O’Valle, F. et al. Relationship between periodontal parameters and plasma cytokine profiles in pregnant woman with preterm birth or low birth weight. Clin Oral Invest 20, 669–674 (2016). https://doi.org/10.1007/s00784-015-1553-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-015-1553-x

Keywords

Search

Navigation