Maternal Periodontal Disease is Associated with Oxidative Stress during Pregnancy

ABSTRACT

We sought to determine if maternal periodontal disease is associated with oxidative stress as measured by serum 8-isoprostane. A secondary analysis was conducted using prospective data from the Oral Conditions and Pregnancy Study. Healthy women enrolled at < 26 weeks' gestational age underwent oral examination and serum sampling. Maternal periodontal disease status was categorized as healthy, mild, or moderate to severe by clinical criteria. Maternal serum was analyzed for 8-isoprostane using ultrasensitive enzyme-linked immunosorbent assay. Elevated 8-isoprostane level was defined as ≥ 75th percentile. Maternal factors associated with elevated 8-isoprostane were determined using chi-square or t test. Multivariable logistic regression was used to assess association between elevated 8-isoprostane and maternal factors. Seven hundred ninety-one women had complete data. Median (interquartile) 8-isoprostane serum level was 1806 (16 to 81,870) pg/dL. Using bivariate analysis, maternal age, race, marital status, utilization of public assistance, and mild or moderate to severe periodontal disease were associated with elevated serum 8-isoprostane. Using logistic regression, moderate to severe periodontal disease (adjusted odds ratio 2.9, 95% confidence interval: 1.7 to 5.0) remained significantly associated with an elevated serum 8-isoprostane level. Maternal periodontal disease is associated with oxidative stress during pregnancy. Further study is needed to determine the role of maternal oxidative stress in periodontal disease-associated adverse pregnancy outcomes.

KEYWORDS

Periodontal disease - oxidative stress - pregnancy - 8-isoprostane - biomarker

REFERENCES

• 1 Chapple I L. Reactive oxygen species and antioxidants in inflammatory diseases.  J Clin Periodontol. 1997;  24 287-296
• 2 Milne G L, Yin H, Brooks J D, Sanchez S, Jackson Roberts II L, Morrow J D. Quantification of F2-isoprostanes in biological fluids and tissues as a measure of oxidant stress.  Methods Enzymol. 2007;  433 113-126
• 3 Borges Jr I, Moreira E A, Filho D W, de Oliveira T B, da Silva M B, Fröde T S. Proinflammatory and oxidative stress markers in patients with periodontal disease.  Mediators Inflamm. 2007;  2007 45794
• 4 Panjamurthy K, Manoharan S, Ramachandran C R. Lipid peroxidation and antioxidant status in patients with periodontitis.  Cell Mol Biol Lett. 2005;  10 255-264
• 5 Chapple I L, Matthews J B. The role of reactive oxygen and antioxidant species in periodontal tissue destruction.  Periodontol 2000. 2007;  43 160-232
• 6 Boggess K A, Lieff S, Murtha A P, Moss K, Beck J, Offenbacher S. Maternal periodontal disease is associated with an increased risk for preeclampsia.  Obstet Gynecol. 2003;  101 227-231
• 7 Uotila J, Tuimala R, Pyykkö K, Ahotupa M. Pregnancy-induced hypertension is associated with changes in maternal and umbilical blood antioxidants.  Gynecol Obstet Invest. 1993;  36 153-157
• 8 Hubel C A. Oxidative stress in the pathogenesis of preeclampsia.  Proc Soc Exp Biol Med. 1999;  222 222-235
• 9 Chappell L C, Seed P T, Briley A et al.. A longitudinal study of biochemical variables in women at risk of preeclampsia.  Am J Obstet Gynecol. 2002;  187 127-136
• 10 Wikström A K, Nash P, Eriksson U J, Olovsson M H. Evidence of increased oxidative stress and a change in the plasminogen activator inhibitor (PAI)-1 to PAI-2 ratio in early-onset but not late-onset preeclampsia.  Am J Obstet Gynecol. 2009;  201 597 e1-e8
• 11 Lieff S, Boggess K A, Murtha A P et al.. The oral conditions and pregnancy study: periodontal status of a cohort of pregnant women.  J Periodontol. 2004;  75 116-126
• 12 Morrow J D, Harris T M, Roberts II L J. Noncyclooxygenase oxidative formation of a series of novel prostaglandins: analytical ramifications for measurement of eicosanoids.  Anal Biochem. 1990;  184 1-10
• 13 Montuschi P, Barnes P J, Roberts II L J. Isoprostanes: markers and mediators of oxidative stress.  FASEB J. 2004;  18 1791-1800
• 14 Xiong X, Buekens P, Fraser W D, Beck J, Offenbacher S. Periodontal disease and adverse pregnancy outcomes: a systematic review.  BJOG. 2006;  113 135-143
• 15 Shub A, Swain J R, Newnham J P. Periodontal disease and adverse pregnancy outcomes.  J Matern Fetal Neonatal Med. 2006;  19 521-528
• 16 Siqueira F M, Cota L O, Costa J E, Haddad J P, Lana A M, Costa F O. Maternal periodontitis as a potential risk variable for preeclampsia: a case-control study.  J Periodontol. 2008;  79 207-215
• 17 Shub A, Wong C, Jennings B, Swain J R, Newnham J P. Maternal periodontal disease and perinatal mortality.  Aust N Z J Obstet Gynaecol. 2009;  49 130-136
• 18 Srinivas S K, Sammel M D, Stamilio D M et al.. Periodontal disease and adverse pregnancy outcomes: is there an association?.  Am J Obstet Gynecol. 2009;  200 497 e1-e8
• 19 Manau C, Echeverria A, Agueda A, Guerrero A, Echeverria J J. Periodontal disease definition may determine the association between periodontitis and pregnancy outcomes.  J Clin Periodontol. 2008;  35 385-397
• 20 Horton A L, Boggess K A, Moss K L, Jared H L, Beck J, Offenbacher S. Periodontal disease early in pregnancy is associated with maternal systemic inflammation among African American women.  J Periodontol. 2008;  79 1127-1132
• 21 Ruma M, Boggess K, Moss K et al.. Maternal periodontal disease, systemic inflammation, and risk for preeclampsia.  Am J Obstet Gynecol. 2008;  198 389 e1-e5
• 22 Barden A, Beilin L J, Ritchie J, Croft K D, Walters B N, Michael C A. Plasma and urinary 8-iso-prostane as an indicator of lipid peroxidation in pre-eclampsia and normal pregnancy.  Clin Sci (Lond). 1996;  91 711-718
• 23 Offenbacher S, Beck J D, Jared H L Maternal Oral Therapy to Reduce Obstetric Risk (MOTOR) Investigators et al. Effects of periodontal therapy on rate of preterm delivery: a randomized controlled trial.  Obstet Gynecol. 2009;  114 551-559
• 24 Macones G A, Parry S, Nelson D B et al.. Treatment of localized periodontal disease in pregnancy does not reduce the occurrence of preterm birth: results from the Periodontal Infections and Prematurity Study (PIPS).  Am J Obstet Gynecol. 2010;  202 147 e1-e8
• 25 Gilbert G H, Duncan R P, Shelton B J. Social determinants of tooth loss.  Health Serv Res. 2003;  38 (6 Pt 2) 1843-1862
• 26 Christensen L B, Petersen P E, Steding-Jessen M. Consumption of dental services among adults in Denmark 1994-2003.  Eur J Oral Sci. 2007;  115 174-179
• 27 Wamala S, Merlo J, Boström G. Inequity in access to dental care services explains current socioeconomic disparities in oral health: the Swedish National Surveys of Public Health 2004-2005.  J Epidemiol Community Health. 2006;  60 1027-1033