Skip to main content

Advertisement

Log in

Interaction between stress, cytokines, and salivary cortisol in pregnant and non-pregnant women with gingivitis

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

Abstract

Objectives

The aim of this study was to compare the effects of periodontal treatment on the inflammatory markers in gingival crevicular fluid and the concentration of salivary cortisol between non-pregnant and pregnant women with gingivitis.

Materials and methods

This study included 30 non-pregnant women (mean age 27.93 ± 6.61 years) and 30 pregnant women (mean age 28.93 ± 4.04 years). Each participant presented with the clinical symptoms of generalized, moderate-to-severe gingivitis. Saliva samples were collected by using the spitting method, and gingival crevicular fluid (GCF) samples were collected by using the intrasulcular method at baseline and after 3 weeks. Non-surgical periodontal treatment (NPT) comprising scaling and oral hygiene instruction was administered after sample collection. The interleukin-6 and interleukin-10 levels in GCF and salivary cortisol concentrations were determined with using enzyme-linked immunosorbent assay.

Results

The pregnant women exhibited significantly deeper pockets (p < 0.05) and greater gingival inflammation (p < 0.05) than the non-pregnant women after periodontal therapy. Moreover, the levels of interleukin-6 in the GCF were significantly higher in the pregnant women compared to the non-pregnant women after periodontal therapy: 17.73 ± 9.82 pg per site and 8.08 ± 4.51 pg per site, respectively, p < 0.05. No differences in the levels of interleukin-10 were observed. The pregnant women also exhibited higher cortisol concentration in the saliva after periodontal therapy, compared to the non-pregnant women, while the levels of stress (as seen on the perceived stress scale-10) were similar in both groups.

Conclusions

Although non-surgical periodontal therapy may reduce the clinical parameters of gingivitis, increasing levels of stress in pregnancy may reduce the individual’s response to it. However, further studies are necessary to substantiate these early findings.

Clinical relevance

Psychosocial stress may increase the risk of periodontal disease by altering the behavioral and immune responses of the individual. Therefore, the levels of stress should be taken into consideration in order to increase the efficacy of periodontal therapy in pregnant patients.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Notes

  1. Hu-Friedy Co., Chicago, IL

  2. Periopaper, Oraflow Inc., Amitville, NY

  3. E-Bioscience, Biomedical Research Center, San Diego, CA

  4. DRG Salivary Cortisol, DRG International, Inc., NJ

  5. IBM SPSS Statistics 19, SPSS Inc., Somers, NY

References

  1. Mengel R, Bacher M, Flores-de-Jacoby L (2002) Interactions between stress, interleukin-1β, interleukin-6 and cortisol in periodontally diseased patients. J Clin Periodontol 29:1012–1022

    Article  PubMed  Google Scholar 

  2. Deinzer R, Granrath N, Spahl M, Linz S, Waschul B, Herforth A (2005) Stress, oral health behaviour and clinical outcome. Br J Health Psychol 10:269–283

    Article  PubMed  Google Scholar 

  3. Stabholz A, Soskolne WA, Shapira L (2010) Genetic and environmental risk factors for chronic periodontitis and aggressive periodontitis. Periodontol 2000(53):138–153

    Article  Google Scholar 

  4. Marcenes WS, Sheiham A (1992) The relationship between work stress and oral health status. Soc Sci Med 35:1511–1520

    Article  PubMed  Google Scholar 

  5. Breivik T, Thrane PS, Murison R, Gjermo P (1996) Emotional stress effects on immunity, gingivitis and periodontitis. Eur J Oral Sci 104:327–334

    Article  PubMed  Google Scholar 

  6. Backé E-M, Seidler A, Latza U, Rossnagel K, Schumann B (2012) The role of psychosocial stress at work for the development of cardiovascular diseases: a systematic review. Int Arch Occup Environ Health 85:67–79

    Article  PubMed  Google Scholar 

  7. Silva A, Newman H, Oakley D (1995) Psychosocial factors in inflammatory periodontal diseases. J Clin Periodontol 22:516–526

    Article  PubMed  Google Scholar 

  8. Cohen S, Williamson GM (1991) Stress and infectious disease in humans. Psychol Bull 109:5–24

    Article  PubMed  Google Scholar 

  9. Preeja C, Ambili R, Nisha KJ, Seba A, Archana V (2013) Unveiling the role of stress in periodontal etiopathogenesis: an evidence-based review. J Investig Clin Dent 4:78–83

    Article  PubMed  Google Scholar 

  10. Aardal E, Holm A-C (1995) Cortisol in saliva-reference ranges and relation to cortisol in serum. Clin Chem Lab Med 33:927–932

    Article  Google Scholar 

  11. Axtelius B, Söderfeldt B, Nilsson A, Edwardsson S, Attström R (1998) Therapy-resistant periodontitis. Psychosocial characteristics. J Clin Periodontol 25:482–491

    Article  PubMed  Google Scholar 

  12. Dickerson SS, Kemeny ME (2004) Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. Psychol Bull 130:355–391

    Article  PubMed  Google Scholar 

  13. Soeda R, Tasaka A, Sakuraı K (2012) Influence of chewing force on salivary stress markers as indicator of mental stress. J Oral Rehabil 39:261–269

    Article  PubMed  Google Scholar 

  14. Cakmak O, Tasdemir Z, Aral CA, Dundar S, Koca HB (2016) Gingival crevicular fluid and saliva stress hormone levels in patients with chronic and aggressive periodontitis. J Clin Periodontol 43:1024–1031

    Article  PubMed  Google Scholar 

  15. Kiecolt-Glaser JK, Preacher KJ, MacCallum RC, Atkinson C, Malarkey WB, Glaser R (2003) Chronic stress and age-related increases in the proinflammatory cytokine IL-6. Proc Natl Acad Sci U S A 100:9090–9095

    Article  PubMed  PubMed Central  Google Scholar 

  16. Gejrot T, Fluur E, Levi L (1967) Sympatho-adrenomedullary activity during experimentally provoked mental stress in patients with labyrinthine defects. Acta Otolaryngol 63:260–267

    Article  Google Scholar 

  17. Snyder DS, Unanue ER (1982) Corticosteroids inhibit murine macrophage Ia expression and interleukin 1 production. J Immunol 129:1803–1805

    PubMed  Google Scholar 

  18. Raber-Durlacher J, Steenbergen T, Velden U, Graaff J, Abraham-Inpijn L (1994) Experimental gingivitis during pregnancy and post-partum: clinical, endocrinological, and microbiological aspects. J Clin Periodontol 21:549–558

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  21. Tilakaratne A, Soory M, Ranasinghe A, Corea S, Ekanayake S, Silva M (2000) Periodontal disease status during pregnancy and 3 months post-partum, in a rural population of Sri-Lankan women. J Clin Periodontol 27:787–792

    Article  PubMed  Google Scholar 

  22. Sooriyamoorthy M, Gower D (1989) Hormonal influences on gingival tissue: relationship to periodontal disease. J Clin Periodontol 16:201–208

    Article  PubMed  Google Scholar 

  23. Huizink AC (2001) Prenatal stress and its effect on infant development. Thesis. Utrecht University, Utrecht, Nederland

  24. Van den Berg B (1992) Maternal emotions during pregnancy and fetal and neonatal behavior. In: Fetal behavior. Development and perinatal aspects. Oxford Univ. Press, Oxford

    Google Scholar 

  25. Mulder EJ, De Medina PR, Huizink AC, Van den Bergh BR, Buitelaar JK, Visser GH (2002) Prenatal maternal stress: effects on pregnancy and the (unborn) child. Early Hum Dev 70:3–14

    Article  PubMed  Google Scholar 

  26. Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4:1–6

    Article  PubMed  Google Scholar 

  27. Silness J, Löe H (1964) Periodontal disease in pregnancy II. Correlation between oral hygiene and periodontal condition. Acta Odontol Scand 22:121–135

    Article  PubMed  Google Scholar 

  28. Löe H (1967) The gingival index, the plaque index and the retention index systems. J Periodontol 38:610–616

    Article  Google Scholar 

  29. Yalcin F, Eskinazi E, Soydinc M et al (2002) The effect of sociocultural status on periodontal conditions in pregnancy. J Periodontol 73:178–182

    Article  PubMed  Google Scholar 

  30. Eskin M, Harlak H, Demirkıran F, Dereboy Ç (2013) The adaptation of the perceived stress scale into Turkish: a reliability and validity analysis. New Symp J 51:132–140

    Google Scholar 

  31. Redmond N, Richman J, Gamboa CM et al (2013) Perceived stress is associated with incident coronary heart disease and all-cause mortality in low-but not high-income participants in the reasons for geographic and racial differences in stroke study. J Am Heart Assoc 2:e000447

    Article  PubMed  PubMed Central  Google Scholar 

  32. Khosravisamani M, Maliji G, Seyfi S et al (2014) Effect of the menstrual cycle on inflammatory cytokines in the periodontium. J Periodontal Res 49:770–776

    Article  PubMed  Google Scholar 

  33. Refulio Z, Rocafuerte M, de la Rosa M, Mendoza G, Chambrone L (2013) Association among stress, salivary cortisol levels, and chronic periodontitis. J Periodontal Implant Sci 43:96–100

    Article  PubMed  PubMed Central  Google Scholar 

  34. Haririan H, Bertl K, Laky M et al (2012) Salivary and serum chromogranin a and α-amylase in periodontal health and disease. J Periodontol 83:1314–1321

    Article  PubMed  Google Scholar 

  35. Offenbacher S, Lin D, Strauss R et al (2006) Effects of periodontal therapy during pregnancy on periodontal status, biologic parameters, and pregnancy outcomes: a pilot study. J Periodontol 77:2011–2024

    Article  PubMed  Google Scholar 

  36. Fiorini T, Susin C, da Rocha JM et al (2013) Effect of nonsurgical periodontal therapy on serum and gingival crevicular fluid cytokine levels during pregnancy and postpartum. J Periodontal Res 48:126–133

    Article  PubMed  Google Scholar 

  37. Michalowicz BS, Novak MJ, Hodges JS et al (2009) Serum inflammatory mediators in pregnancy: changes after periodontal treatment and association with pregnancy outcomes. J Periodontol 80:1731–1741

    Article  PubMed  PubMed Central  Google Scholar 

  38. Çorumlu EP, Ulupınar E.(2016) Neurobiological effects of prenatal stress exposure. Osmangazi J Med 38

  39. Van den Bergh B (1990) The influence of maternal emotions during pregnancy on fetal and neonatal behavior. Pre-and Perinatal Psychology J 5:119–130

    Google Scholar 

  40. Coussons-Read ME, Okun ML, Nettles CD (2007) Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav Immun 21:343–350

    Article  PubMed  Google Scholar 

  41. Christian LM, Glaser R, Porter K, Iams JD (2013) Stress-induced inflammatory responses in women: effects of race and pregnancy. Psychosom Med 75:658–669

    Article  PubMed  PubMed Central  Google Scholar 

  42. Giannopoulou C, Kamma JJ, Mombelli A (2003) Effect of inflammation, smoking and stress on gingival crevicular fluid cytokine level. J Clin Periodontol 30:145–153

    Article  PubMed  Google Scholar 

  43. Kamma JJ, Giannopoulou C, Vasdekis VG, Mombelli A (2004) Cytokine profile in gingival crevicular fluid of aggressive periodontitis: influence of smoking and stress. J Clin Periodontol 31:894–902

    Article  PubMed  Google Scholar 

  44. Aurer A, Aurer-Kozelj J, Stavljenic-Rukavina A, Kalenic S, Ivic-Kardum M, Haban V (1999) Inflammatory mediators in saliva of patients with rapidly progressive periodontitis during war stress induced incidence increase. Coll Antropol 23:117–124

    PubMed  Google Scholar 

  45. Paik IH, Toh KY, Lee C, Kim JJ, Lee SJ (2000) Psychological stress may induce increased humoral and decreased cellular immunity. Behav Med 26:139–141

    Article  PubMed  Google Scholar 

  46. Johannsen A, Rylander G, Söder B, Marie Å (2006) Dental plaque, gingival inflammation, and elevated levels of interleukin-6 and cortisol in gingival crevicular fluid from women with stress-related depression and exhaustion. J Periodontol 77:1403–1409

    Article  PubMed  Google Scholar 

  47. Chrousos GP (1995) The hypothalamic–pituitary–adrenal axis and immune-mediated inflammation. N Engl J Med 332:1351–1363

    Article  PubMed  Google Scholar 

  48. Ishisaka A, Ansai T, Soh I et al (2008) Association of cortisol and dehydroepiandrosterone sulphate levels in serum with periodontal status in older Japanese adults. J Clin Periodontol 35:853–861

    Article  PubMed  Google Scholar 

  49. Locker D, Leake J (1993) Risk indicators and risk markers for periodontal disease experience in older adults living independently in Ontario, Canada. J Dent Res 72:9–17

    Article  PubMed  Google Scholar 

  50. Genco RJ, Ho AW, Grossi SG, Dunford RG, Tedesco LA (1999) Relationship of stress, distress, and inadequate coping behaviors to periodontal disease. J Periodontol 70:711–723

    Article  PubMed  Google Scholar 

  51. Cakmak O, Alkan BA, Ozsoy S, Sen A, Abdulrezzak U (2014) Association of gingival crevicular fluid cortisol/dehydroepiandrosterone levels with periodontal status. J Periodontol 85:e287–e294

    Article  PubMed  Google Scholar 

  52. González-Cabrera J, Fernández-Prada M, Iribar-Ibabe C, Peinado JM (2014) Acute and chronic stress increase salivary cortisol: a study in the real-life setting of a national examination undertaken by medical graduates. Stress 17:149–156

    Article  PubMed  Google Scholar 

  53. Shelton MM, Schminkey DL, Groer MW (2015) Relationships among prenatal depression, plasma cortisol, and inflammatory cytokines. Biol Res Nurs 17:295–302

    Article  PubMed  Google Scholar 

  54. Kaur M, Geisinger ML, Geurs NC et al (2014) Effect of intensive oral hygiene regimen during pregnancy on periodontal health, cytokine levels, and pregnancy outcomes: a pilot study. J Periodontol 85:1684–1692

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This study was supported by the Gaziosmanpasa University Scientific Research Projects Office, Tokat, Turkey with the project number 2015/130. The authors are grateful to Gaziosmanpasa University Scientific Research Projects Office for their substantial support.

Funding

The work was supported by the Gaziosmanpasa University Scientific Research Projects Office, Tokat, Turkey with the project number 2015/130.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ozge Gokturk.

Ethics declarations

The study protocol was approved by the Ethical Committee, Faculty of Dentistry, Gaziosmanpasa University.

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yarkac, F.U., Gokturk, O. & Demir, O. Interaction between stress, cytokines, and salivary cortisol in pregnant and non-pregnant women with gingivitis. Clin Oral Invest 25, 1677–1684 (2021). https://doi.org/10.1007/s00784-018-2569-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-018-2569-9

Keywords

Navigation