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Obstetrics & Gynecology:
Original Research

Maternal Periodontal Disease Is Associated With an Increased Risk for Preeclampsia

Boggess, Kim A. MD; Lieff, Susi PhD; Murtha, Amy P. MD; Moss, Kevin; Beck, James PhD; Offenbacher, Steven DDS, PhD

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Author Information

Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, and Center for Oral and Systemic Diseases, University of North Carolina, Chapel Hill, North Carolina; and Department of Obstetrics and Gynecology, Duke University Medical Center, Durham, North Carolina.

Address reprint requests to: Kim A. Boggess, MD, University of North Carolina School of Medicine, Department of Obstetrics and Gynecology, Division of Maternal-Fetal Medicine, CB #7516, Chapel Hill, NC 27599; E-mail: kboggess@med.unc.edu.

This study was supported by National Institute of Dental and Craniofacial Research grant no. DE-012453.

Received May 13, 2002. Received in revised form July 2, 2002. Accepted August 1, 2002.

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Abstract

OBJECTIVE: To determine if maternal periodontal disease is associated with the development of preeclampsia.

METHODS: A cohort of 1115 healthy pregnant women were enrolled at less than 26 weeks' gestation and followed until delivery. Maternal demographic and medical data were collected. Periodontal examinations were performed at enrollment and within 48 hours of delivery to determine the presence of severe periodontal disease or periodontal disease progression. Preeclampsia was defined as blood pressure greater than 140/90 on two separate occasions, and at least 1+ proteinuria on catheterized urine specimen. The potential effects of maternal age, race, smoking, gestational age at delivery, and insurance status were analyzed, and adjusted odds ratios for preeclampsia were calculated using multivariable logistic regression.

RESULTS: During the study period, 763 women delivered live infants and had data available for analysis. Thirty-nine women had preeclampsia. Women were at higher risk for preeclampsia if they had severe periodontal disease at delivery (adjusted odds ratio 2.4, 95% confidence interval 1.1, 5.3), or if they had periodontal disease progression during pregnancy (adjusted odds ratio 2.1, 95% confidence interval 1.0, 4.4).

CONCLUSION: After adjusting for other risk factors, active maternal periodontal disease during pregnancy is associated with an increased risk for the development of preeclampsia.

Preeclampsia is a common hypertensive disorder of pregnancy, affecting 5–10% of pregnancies and contributing significantly to maternal and perinatal morbidity and mortality. Despite the impact of this condition, efforts at understanding the etiologic factors and measures designed to prevent or treat preeclampsia have been disappointing. Although several etiologies have been proposed, a common final pathway is likely. Preeclampsia and atherosclerosis share some common epidemiologic risk factors, and placental pathologic changes similar to atherosclerotic vascular changes have been described.1,2 Endothelial damage in the placental vascular bed may be initiated by a number of mechanisms. This damage results in oxidative and inflammatory vascular damage, which may ultimately result in the development of preeclampsia.3 A major question yet to be addressed is the initiating factor for this pathologic process.

Chronic oral infections have been implicated as causative agents in a variety of systemic illnesses including atherosclerotic cardiovascular disease and cerebrovascular ischemia.4–6 In addition, periodontal disease has also been associated with adverse pregnancy outcomes. In a case-control study, we found that maternal periodontal disease was associated with delivery of a preterm low birth weight infant.7 In a prospective study of over 1000 women, Jeffcoat et al have recently demonstrated that women with severe periodontal disease detected at mid-pregnancy were at increased risk for preterm delivery, even after adjusting for potential other risk factors, with risk greatest for delivery at less than 32 weeks' gestation.8 Given the similarity between placental vascular damage and atherosclerosis, and the potential for chronic oral infection to affect systemic organ systems, we sought to examine whether an association exists between maternal periodontal disease and the development of preeclampsia.

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MATERIALS AND METHODS

The Oral Conditions and Pregnancy study was a prospective cohort study of the effect of maternal periodontal disease on obstetric outcome conducted by the University of North Carolina Center for Oral and Systemic Disease and the Center for Inflammatory Disorders, in collaboration with Duke University Medical Center Institutional Review Board approval was obtained to conduct the study, and participants gave written informed consent to participate. Eligible women were identified at their first or second prenatal visit and enrolled before 26 weeks' gestation. Women were excluded from participation if less than 18 years of age without a legal guardian, were greater than 26 weeks' gestation at study enrollment, had a multiple gestation, chronic hypertension, pregestational diabetes, heart murmur or heart valve disease, history of fenfluramine-phentermine use (unless a normal echocardiogram was documented), any medical condition requiring antibiotic prophylaxis for dental treatment, human immunodeficiency virus infection, or delivery was planned at another institution. A tracking system was used to record recruitment and enrollment to determine eligibility, enrollment, and attrition rates (Epi Info 6.0, Centers for Disease Control and Prevention, Atlanta, GA). Preeclampsia was defined as blood pressure greater than 140/90 on two separate occasions, and at least 1+ proteinuria on catheterized urine specimen. The potential effects of maternal age, race, smoking, gestational age at delivery, and insurance status were analyzed, and adjusted odds ratios for preeclampsia were calculated using multivariable logistic regression.

Demographic, health behavior, and medical history data were obtained by patient questionnaire at the first visit and were reviewed by a physician at the first prenatal visit. Information on events of the pregnancy, labor and delivery, and health of the neonate were collected from the medical record, laboratory and pathology data, and the infant's medical record and entered in the Oral Conditions and Pregnancy Study database (Microsoft Access, 1997 SR2, Microsoft, Redmond, WA).

An oral health examination was performed at the first or second prenatal visit and then repeated within 48 hours antepartum. Five certified dental hygienist examiners were trained by a standard examiner and calibrated at the start of the study and at 6-month intervals, using pocket depth and attachment loss measurements. All weighted κ scores were greater than 85%, and intraclass correlation coefficients were 0.90 or higher. A screening examination of the mouth was done to assess for the presence of suspicious oral lesions or conditions requiring referral to a dentist. Several measures of periodontal health were then collected: gingival pocket depth, gingival recession, and tooth attachment loss. Gingival pocket depth was measured in millimeters with a UNC-15 periodontal probe at six sites per tooth as the distance from the gingival margin to the periodontal ligament attachment. Gingival recession was determined by measuring the distance from the cementoenamel junction to the gingival margin in millimeters and rounded down to the next millimeter. Tooth attachment loss was calculated from recession and pocket depth measures and represented the distance in millimeters from the cementoenamel junction to periodontal ligament attachment.

For the purpose of this analysis, periodontal health or the absence of periodontal disease was defined as absence of gingival pocket depths greater than or equal to 4-mm pocket depth and absence of attachment loss 3 mm or more, with no bleeding on probing. Mild periodontal disease was defined as one or more tooth sites with greater than or equal to 4-mm pocket depth or one or more tooth pockets that bled on probing, up to 15 tooth sites. Severe periodontal disease was defined as 15 or more tooth sites with pocket depths greater than or equal to 4 mm. Disease progression was defined as four or more sites that increased 2 mm or more in pocket depth, resulting in pockets of 4 mm or more in depth.

Bivariate analysis was performed on a priori candidate confounders to determine association with the development of preeclampsia using the χ2 test. All variables were tested for confounding by testing to see if the odds ratio for preeclampsia changed by 10% or more by inclusion of that variable in the model. All variables that were determined to be confounders or were variables of interest (ie, smoking) were then entered into a multivariable logistic regression model and then removed in a stepwise fashion if P < 2 by the backward elimination procedure. All variables included in the final models were determined to be independent by assessing collinearity by computing the eigenvalue.9 All analyses were performed using Statistical Analytical Systems 8.0 (SAS Institute, Cary, NC).

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RESULTS

During the study period, 5400 women received prenatal care at the study site, and 3456 (64%) of those women were ineligible. Of the 1944 eligible women, 1115 (57%) agreed to participate in the study. Two hundred thirty (20.6%) were excluded from the analysis because they withdrew (109), became ineligible (38), or experienced a spontaneous (72) or elective abortion (11). Of 885 remaining women, 16 (1.9%) experienced either an intrauterine fetal (13) or neonatal (three) demise. The incidence of preeclampsia was 4.4% (39 of 885). Of the 869 women enrolled and having live births, 850 (98.3%) had enrollment oral examinations performed, and 763 (87.8%) had delivery examinations. All 763 women with delivery examinations also had an enrollment oral examination, and periodontal disease progression was assessed in this group. At enrollment, 229 (26.9%) of 850 women who had oral examinations performed had no periodontal disease, 496 (58.4%) had mild disease, and 125 (14.7) had severe disease. At delivery, 378 (49.5%) of 763 women who had oral examinations performed had no periodontal disease, 285 (37.3%) had mild disease, and 100 (13.1%) had severe disease. Periodontal disease progression occurred in 203 (26.6%) of 763 women who had both enrollment and delivery oral examinations.

Maternal demographic characteristics, obstetric data, and periodontal disease status are shown in Table 1. Variables found to be associated with preeclampsia (P ≤ .2) (maternal age, race, having insurance, delivery less than 37 weeks' gestation, and periodontal disease at delivery) were then included in the multivariable logistic regression model. Smoking during pregnancy, although not associated with preeclampsia in our cohort, has been found to be protective against the development of preeclampsia in other studies,10,11 and was included in the model. Variables were then removed from the model in a backward elimination procedure by P ≤ .2, with smoking forced to remain. The final model generated by this method included severe periodontal disease, delivery at less than 37 weeks' gestation, and smoking. Severe periodontal disease at delivery was associated with an increased odds ratio for preeclampsia (adjusted odds ratio 2.4, 95% confidence interval 1.1, 5.3). A separate model was generated to assess the main effect of periodontal disease progression on the development of preeclampsia. Using the backward elimination procedure, periodontal disease progression was also associated with an increased odds ratio for the development of preeclampsia (odds ratio 2.1, 95% confidence interval 1.0, 4.4). There was no collinearity between variables included in the final model.

Table 1
Table 1
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DISCUSSION

Maternal clinical periodontal disease at delivery is associated with an increased risk for the development of preeclampsia, independent of the effects of maternal age, race, smoking, gestational age at delivery, and insurance status. In addition, clinically active disease, as measured by presence of periodontal disease progression, is also associated with an increased risk for preeclampsia.

A parallel between the pathophysiologic consequences of preeclampsia and atherosclerotic disease has been suggested.12 Atherosclerosis, like preeclampsia, is associated with endothelial dysfunction, which may be caused by oxidative stress and subsequent lipid peroxidation, hyperlipidemia,13 or hyperhomocysteinemia.14 Molecular variants in the angiotensinogen gene have been associated with both atherosclerosis15 and preeclampsia,16 and several epidemiologic factors predispose to the development of both atherosclerosis and preeclampsia: obesity, black race, and preexisting hypertension. However, despite the similarities between atherosclerosis and preeclampsia, little is known about potential common putative factors.

Recently, an intriguing etiologic factor related to atherosclerosis has been identified that may contribute to the development of adverse pregnancy outcomes. Periodontal disease, a chronic oral gram-negative infection, has been associated with atherosclerosis, thromboembolic events,4,5,17 and hypercholesterolemia.18 In addition, oral pathogens have been detected in atherosclerotic plaques, where they can play a role in the development and progression of atherosclerosis leading to coronary vascular disease.19 Periodontal disease may provide a chronic burden of endotoxin and inflammatory cytokines, which serve to initiate and exacerbate atherogenesis and thrombogenesis. It is possible that the placenta may be similarly burdened in pregnant women who develop preeclampsia.

Periodontal disease is characterized by periods of exacerbation interspersed with periods of remission and presents a local microbial burden that initiates local inflammation and local tissue destruction.20 We hypothesize that women with active periodontal disease during pregnancy may have transient translocation of oral organisms to the uteroplacental unit, inciting placental inflammation or oxidative stress early in pregnancy, which ultimately produces placental damage and the clinical manifestation of preeclampsia. A subset of this cohort of women has had umbilical cord serum assessed for the presence of fetal immunoglobulin M to oral pathogens. Fifty-seven (16%) of 351 fetal cord blood samples collected demonstrate fetal immunoglobulin M to the oral pathogen Porphyromonas gingivalis, documenting a fetal humoral response to organisms distant from the intrauterine environment21 and suggesting that translocation of oral pathogens to the uteroplacental unit may occur.

Caution should be exercised when interpreting these data, as the etiology of both periodontal disease and preeclampsia is likely multifactorial. Maternal periodontal disease may also represent a surrogate for another maternal factor that predisposes to the development of preeclampsia. Further study on the maternal and fetal inflammatory responses to chronic oral infection and on placental pathology in women with periodontal disease is ongoing to determine whether the relationship between periodontal disease and preeclampsia is causal or simply associative. If the relationship between maternal periodontal disease and preeclampsia risk proves causal in nature, then treatment of periodontal disease during pregnancy may represent a novel approach to the prevention of preeclampsia.

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REFERENCES

1. Khong TY, Mott C. Immunohistologic demonstration of endothelial disruption in acute atherosis in pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 1993;51:193–7.

2. Ramos JG, Martins-Costa S, Edelweiss MI, Costa CA. Placental bed lesions and infant birth weight in hypertensive pregnant women. Braz J Med Biol Res 1995;28:447–55.

3. Dekker GA, Sibai BM. The immunology of preeclampsia. Semin Perinatol 1999;23:24–33.

4. Beck JD, Pankow J, Tyroler HA, Offenbacher S. Dental infections and atherosclerosis. Am Heart J 1999;138:528–33.

5. Beck JD, Offenbacher S, Williams R, Gibbs P, Garcia R. Periodontitis: A risk factor for coronary heart disease? Ann Periodontol 1998;3:127–41.

6. Mercado F, Marshall RI, Klestov AC, Bartold PM. Is there a relationship between rheumatoid arthritis and periodontal disease? J Clin Periodontol 2000;27:267–72.

7. Offenbacher S, Jared HL, O'Reilly PG, Wells SR, Salvi GE, Lawrence HP, et al. Potential pathogenic mechanisms of periodontitis associated pregnancy complications. Ann Periodontol 1998;3:233–50.

8. Jeffcoat M, Geurs N, Reddy M, Cliver S, Goldenberg R, Hauth J. Periodontal infection and preterm birth: Results of a prospective study. J Amer Dent Assoc 2001;132:875–80.

9. Kleinbaum D, Kupper L, Muller K. Applied regression analysis and other multivariable methods. Belmont, CA: Wadsworth Publishing, 1998.

10. Cnattingius S, Mills JL, Yuen J, Eriksson O, Salonen H The paradoxical effect of smoking in preeclamptic pregnancies: Smoking reduces the incidence but increases the rates of perinatal mortality, abruptio placentae, and intrauterine growth restriction. Am J Obstet Gynecol 1997;177:156–61.

11. Zhang J, Klebanoff MA, Levine RJ, Puri M, Moyer P. The puzzling association between smoking and hypertension during pregnancy. Am J Obstet Gynecol 1999;181:1407–13.

12. Sattar N, Bendomir A, Berry C, Shepherd J, Greer IA, Packard CJ. Lipoprotein subfraction concentrations in preeclampsia: Pathogenic parallels to atherosclerosis. Obstet Gynecol 1997;89:403–8.

13. Mylonas C, Kouretas D. Lipid peroxidation and tissue damage. In Vivo 1999;13:295–309.

14. Powers RW, Evans RW, Majors AK, Ojimba JI, Ness RB, Crombleholme WR, et al. Plasma homocysteine concentration is increased in preeclampsia and is associated with evidence of endothelial activation. Am J Obstet Gynecol 1998;179:1605–11.

15. Ishigami T, Umemura S, Iwamoto T, Tamura K, Hibi K, Yamaguchi S, et al. Molecular variant of angiotensinogen gene is associated with coronary atherosclerosis. Circulation 1995;91:951–4.

16. Sibai B. Hypertension in pregnancy. In: Gabbe S, Niebyl J, Simpson J, eds. Obstetrics: Normal and problem pregnancies. New York: Churchill Livingstone, 2001:945–1004.

17. Beck J, Garcia R, Heiss G, Vokonas PS, Offenbacher S Periodontal disease and cardiovascular disease. J Periodontol 1996;67:1123–37.

18. Katz J, Chaushu G, Sharabi Y. On the association between hypercholesterolemia, cardiovascular disease and severe periodontal disease. J Clin Periodontol 2001;28:865–8.

19. Haraszthy VI, Zambon JJ, Trevisan M, Zeid M, Genco RJ Identification of periodontal pathogens in atheromatous plaques. J Periodontol 2000;71:1554–60.

20. Rose L, Genco R, Mealey B, Cohen D. Periodontal medicine. Hamilton, Ontario: B. C. Decker, 2000.

21. Madianos PN, Lieff S, Murtha AP, Boggess KA, Auten RL Jr, Beck JD, et al. Maternal periodontitis and prematurity. Part II: Maternal infection and fetal exposure. Ann Periodontol 2001;6:175–82.

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Coonrod, DV; Jack, BW; Stubblefield, PG; Hollier, LM; Boggess, KA; Cefalo, R; Cox, SN; Dunlop, AL; Hunter, KD; Prasad, MR; Lu, MC; Conry, JA; Gibbs, RS; Hogan, VK
American Journal of Obstetrics and Gynecology, 199(6): S296-S309.
10.1016/j.ajog.2008.08.062
CrossRef
Acta Obstetricia Et Gynecologica Scandinavica
Pregnancy and oral health: utilisation of dental services during pregnancy in northern Greece
Dinas, K; Achyropoulos, V; Hatzipantelis, E; Mavromatidis, G; Zepiridis, L; Theodoridis, T; Dovas, D; Tantanasis, T; Goutzioulis, F; Bontis, J
Acta Obstetricia Et Gynecologica Scandinavica, 86(8): 938-944.
10.1080/00016340701371413
CrossRef
American Journal of Obstetrics and Gynecology
Maternal infection and risk of preeclampsia: Systematic review and metaanalysis
Conde-Agudelo, A; Villar, J; Lindheimer, M
American Journal of Obstetrics and Gynecology, 198(1): 7-22.
10.1016/j.ajog.2007.07.040
CrossRef
Community Dentistry and Oral Epidemiology
Maternal periodontitis and adverse pregnancy outcomes
Pitiphat, W; Joshipura, KJ; Gillman, MW; Williams, PL; Douglass, CW; Rich-Edwards, JW
Community Dentistry and Oral Epidemiology, 36(1): 3-11.
10.1111/j.1600-0528.2006.00363.x
CrossRef
Plos One
Maternal TLR4 and NOD2 Gene Variants, Pro-Inflammatory Phenotype and Susceptibility to Early-Onset Preeclampsia and HELLP Syndrome
van Rijn, BB; Franx, A; Steegers, EAP; de Groot, CJM; Bertina, RM; Pasterkamp, G; Voorbij, HAM; Bruinse, HW; Roest, M
Plos One, 3(4): -.
ARTN e1865
CrossRef
Journal of Periodontology
Maternal Periodontal Disease and Soluble Fms-Like Tyrosine Kinase-1 Expression
Horton, AL; Boggess, KA; Moss, KL; Beck, J; Offenbacher, S
Journal of Periodontology, 80(9): 1506-1510.
10.1902/jop.2009.090189
CrossRef
Journal of Periodontology
Lack of association between periodontal parameters and preeclampsia
Khader, YS; Jibreal, M; Al-Omiri, M; Amarin, Z
Journal of Periodontology, 77(): 1681-1687.
10.1902/jop.2006.050463
CrossRef
Journal of Periodontology
Total antioxidant capacity and antioxidant enzymes in serum, saliva, and gingival crevicular fluid of preeclamptic women with and without Periodontal disease
Canakci, V; Yildirim, A; Canakci, CF; Eltas, A; Cicek, Y; Canakci, H
Journal of Periodontology, 78(8): 1602-1611.
10.1902/jop.2007.060469
CrossRef
Journal of Periodontology
Fetal Exposure to Oral Pathogens and Subsequent Risk for Neonatal Intensive Care Admission
Jared, H; Boggess, KA; Moss, K; Bose, C; Auten, R; Beck, J; Offenbacher, S
Journal of Periodontology, 80(6): 878-883.
10.1902/jop.2009.080642
CrossRef
Maternal and Child Health Journal
Racial disparity in infant and maternal mortality: Confluence of infection, and microvascular dysfunction
Fiscella, K
Maternal and Child Health Journal, 8(2): 45-54.

American Journal of Obstetrics and Gynecology
Chronic maternal and fetal Porphyromonas gingivalis exposure during pregnancy in rabbits
Boggess, KA; Madianos, PN; Preisser, JS; Moise, KJ; Offenbacher, S
American Journal of Obstetrics and Gynecology, 192(2): 554-557.
10.1016/j.ajog.2004.09.001
CrossRef
Journal of Maternal-Fetal & Neonatal Medicine
Provider and patient perceptions about dental care during pregnancy
Strafford, KE; Shellhaas, C; Hade, EM
Journal of Maternal-Fetal & Neonatal Medicine, 21(1): 63-71.
10.1080/14767050701796681
CrossRef
American Journal of Hypertension
Maternal Periodontal Disease and Risk of Preeclampsia: A Case-Control Study
Lohsoonthorn, V; Kungsadalpipob, K; Chanchareonsook, P; Limpongsanurak, S; Vanichjakvong, O; Sutdhibhisal, S; Sookprome, C; Wongkittikraiwan, N; Kamolpornwijit, W; Jantarasaengaram, S; Manotaya, S; Siwawej, V; Barlow, WE; Fitzpatrick, AL; Williams, MA
American Journal of Hypertension, 22(4): 457-463.
10.1038/ajh.2008.365
CrossRef
Oral Diseases
The history of dentistry and medicine relationship: could the mouth finally return to the body?
Vieira, CLZ; Caramelli, B
Oral Diseases, 15(8): 538-546.
10.1111/j.1601-0825.2009.01589.x
CrossRef
Hypertension in Pregnancy
Maternal serum Chlamydia pneumoniae antibodies and CRP levels in women with preeclampsia and gestational hypertension
Karinen, L; Leinonen, M; Bloigu, A; Paldanius, M; Koskela, P; Saikku, P; Hartikainen, AL; Jarvelin, MR; Pouta, A
Hypertension in Pregnancy, 27(2): 143-158.
10.1080/10641950701885188
CrossRef
Plos One
Relationship between Periodontitis and Pre-Eclampsia: A Meta-Analysis
Sgolastra, F; Petrucci, A; Severino, M; Gatto, R; Monaco, A
Plos One, 8(8): -.
ARTN e71387
CrossRef
American Journal of Perinatology
Treatment of Periodontal Disease and Prevention of Preterm Birth: Systematic Review and Meta-analysis
Boutin, A; Demers, S; Roberge, S; Roy-Morency, A; Chandad, F; Bujold, E
American Journal of Perinatology, 30(7): 537-543.
10.1055/s-0032-1329687
CrossRef
Journal of Sexual Medicine
Is There a Relationship Between Chronic Periodontitis and Erectile Dysfunction?
Oguz, F; Eltas, A; Beytur, A; Akdemir, E; Uslu, MO; Gunes, A
Journal of Sexual Medicine, 10(3): 838-843.
10.1111/j.1743-6109.2012.02974.x
CrossRef
Journal of Maternal-Fetal & Neonatal Medicine
Lack of association between maternal periodontal status and adverse pregnancy outcomes: a multicentric epidemiologic study
Abati, S; Villa, A; Cetin, I; Dessole, S; Luglie, PF; Strohmenger, L; Ottolenghi, L; Campus, GG
Journal of Maternal-Fetal & Neonatal Medicine, 26(4): 369-372.
10.3109/14767058.2012.733776
CrossRef
Maternal and Child Health Journal
Racial Disparities in Economic and Clinical Outcomes of Pregnancy Among Medicaid Recipients
Zhang, S; Cardarelli, K; Shim, R; Ye, JL; Booker, KL; Rust, G
Maternal and Child Health Journal, 17(8): 1518-1525.
10.1007/s10995-012-1162-0
CrossRef
Plos One
Periodontal Disease and Risk of Preeclampsia: A Meta-Analysis of Observational Studies
Wei, BJ; Chen, YJ; Yu, L; Wu, B
Plos One, 8(8): -.
ARTN e70901
CrossRef
Journal of Periodontology
Severe Preeclampsia and Maternal Self-Report of Oral Health, Hygiene, and Dental Care
Boggess, KA; Berggren, EK; Koskenoja, V; Urlaub, D; Lorenz, C
Journal of Periodontology, 84(2): 143-151.
10.1902/jop.2012.120079
CrossRef
Periodontology 2000
Bi-directional relationship between pregnancy and periodontal disease
Armitage, GC
Periodontology 2000, 61(): 160-176.
10.1111/j.1600-0757.2011.00396.x
CrossRef
Journal of Obstetrics and Gynaecology Research
Association of maternal periodontal health with adverse pregnancy outcome
Kumar, A; Basra, M; Begum, N; Rani, V; Prasad, S; Lamba, AK; Verma, M; Agarwal, S; Sharma, S
Journal of Obstetrics and Gynaecology Research, 39(1): 40-45.
10.1111/j.1447-0756.2012.01957.x
CrossRef
Journal of Periodontal Research
Increased inflammatory biomarkers in early pregnancy is associated with the development of pre-eclampsia in patients with periodontitis: a case control study
Chaparro, A; Sanz, A; Quintero, A; Inostroza, C; Ramirez, V; Carrion, F; Figueroa, F; Serra, R; Illanes, SE
Journal of Periodontal Research, 48(3): 302-307.
10.1111/jre.12008
CrossRef
American Journal of Therapeutics
Subclinical Infection as a Cause of Inflammation in Preeclampsia
López-Jaramillo, P; Herrera, JA; Arenas-Mantilla, M; Jáuregui, IE; Mendoza, MA
American Journal of Therapeutics, 15(4): 373-376.
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Clinical Obstetrics and Gynecology
Long-Term Outcomes After Preeclampsia
Van Pampus, MG; Aarnoudse, JG
Clinical Obstetrics and Gynecology, 48(2): 489-494.
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Maternal Periodontal Infections, Prematurity, and Growth Restriction
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Progressive Periodontal Disease and Risk of Very Preterm Delivery
Lieff, S; McKaig, RG; Mauriello, SM; Moss, KL; Beck, JD; Offenbacher, S; Boggess, KA; Murtha, AP; Jared, HL
Obstetrics & Gynecology, 107(1): 29-36.
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Obstetrics & Gynecology
Treatment of Periodontal Disease During Pregnancy: A Randomized Controlled Trial
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Obstetrics & Gynecology, 114(6): 1239-1248.
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Journal of Hypertension
Low socioeconomic status is a risk factor for preeclampsia: the Generation R Study
Silva, LM; Coolman, M; Steegers, EA; Jaddoe, VW; Moll, HA; Hofman, A; Mackenbach, JP; Raat, H
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Periodontal disease severity is related to high levels of C-reactive protein in pre-eclampsia
Herrera, JA; Parra, B; Herrera, E; Botero, JE; Arce, RM; Contreras, A; López-Jaramillo, P
Journal of Hypertension, 25(7): 1459-1464.
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Obstetrical & Gynecological Survey
Common Oral Manifestations During Pregnancy: A Review
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Obstetrical & Gynecological Survey
Periodontal Disease and Pregnancy Outcomes: State-of-the-Science
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© 2003 The American College of Obstetricians and Gynecologists

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