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Obstetrics & Gynecology:
doi: 10.1097/01.AOG.0000139836.47777.6d
Original Research

Periodontal Disease and Upper Genital Tract Inflammation in Early Spontaneous Preterm Birth

Goepfert, Alice R. MD*; Jeffcoat, Marjorie K. DMD†; Andrews, William W. PhD, MD*; Faye-Petersen, Ona MD‡; Cliver, Suzanne P.*; Goldenberg, Robert L. MD*; Hauth, John C. MD*

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Author Information

From *The Center for Research in Women's Health and the Department of Obstetrics and Gynecology, The University of Alabama at Birmingham, Birmingham, Alabama; †Department of Periodontology, The University of Pennsylvania School of Dental Medicine, Philadelphia, Pennsylvania; and ‡Department of Pathology, The University of Alabama at Birmingham, Birmingham, Alabama.

This study is supported by the National Institute for Child Health and Human Development, grants P01 HD 33927 and K12 HD01258.

Presented at the 22nd Annual Meeting of the Society for Maternal-Fetal Medicine, January 14–19, 2002, New Orleans, Louisiana.

The authors thank Nico C. Geurs, dmd, and Janatha Grant, rn, for their work on this project.

Reprints are not available. Address reprint correspondence to: Alice R. Goepfert, MD, University of Alabama at Birmingham, Department of Obstetrics and Gynecology, 619 19th Street, South OHB 450, Birmingham, AL 35249–7333; e-mail: aliceg@uab.edu.

Received April 29, 2004. Received in revised form June 27, 2004. Accepted July 1, 2004.

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Abstract

OBJECTIVE: To estimate the relationship between maternal periodontal disease and both early spontaneous preterm birth and selected markers of upper genital tract inflammation.

METHODS: In this case-control study, periodontal assessment was performed in 59 women who experienced an early spontaneous preterm birth at less than 32 weeks of gestation, in a control population of 36 women who experienced an early indicated preterm birth at less than 32 weeks of gestation, and in 44 women with an uncomplicated birth at term (≥ 37 weeks). Periodontal disease was defined by the degree of attachment loss. Cultures of the placenta and umbilical cord blood, cord interleukin-6 levels, and histopathologic examination of the placenta were performed for all women.

RESULTS: Severe periodontal disease was more common in the spontaneous preterm birth group (49%) than in the indicated preterm (25%, P = .02) and term control groups (30%, P = .045). Multivariable analyses, controlling for possible confounders, supported the association between severe periodontal disease and spontaneous preterm birth (odds ratio 3.4, 95% confidence interval 1.5–7.7). Neither histologic chorioamnionitis, a positive placental culture, nor an elevated cord plasma interleukin-6 level was significantly associated with periodontal disease (80% power to detect a 50% difference in rate of histological chorioamnionitis, α = 0.05).

CONCLUSION: Women with early spontaneous preterm birth were more likely to have severe periodontal disease than women with indicated preterm birth or term birth. Periodontal disease was not associated with selected markers of upper genital tract inflammation.

LEVEL OF EVIDENCE: II-2

Preterm birth complicates 12% of all pregnancies in the United States and is one of the leading causes of infant morbidity and mortality.1–2 Evidence indicates that maternal infection and inflammation of the lower and upper genital tract, as well as at sites distant from the pelvis, play a major role in the etiology of preterm birth in some women.3–5

Periodontal disease is a chronic anaerobic inflammatory condition that affects as many as 50% of pregnant women in the United States.6–8 Emerging evidence supports a relationship between periodontal disease and other systemic conditions, including cardiovascular disease and diabetes mellitus.9–11 Recent studies in the United States have demonstrated an association between maternal periodontal disease and multiple adverse pregnancy outcomes, including preterm birth, low birth weight, fetal growth restriction, preeclampsia, and perinatal mortality.6–8,12–16 The mechanisms by which periodontal disease and preterm birth are associated are not clear. It has been hypothesized that in the presence of severe periodontal disease, oral organisms can disseminate hematogenously to target the placenta, membranes, and fetus.17–18 This bacterial challenge may result in increased cytokine expression and precipitate preterm labor.

We sought to determine if women who have a spontaneous preterm birth at less than 32 weeks of gestation are more likely to have periodontal disease than women who have either an indicated preterm birth at less than 32 weeks of gestation or a term birth. In addition, we sought to determine whether selected markers of upper genital tract inflammation were associated with periodontal disease in these women.

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MATERIALS AND METHODS

This case-control study was approved by the Institutional Review Board at the University of Alabama at Birmingham. Women delivering at our institution at between 24 0/7 and 31 6/7 weeks of gestation, as well as women following spontaneous vaginal delivery at term (> 37 weeks) who were enrolled in an ongoing study of risk factors for preterm birth at our institution (Perinatal Emphasis Research Center at the University of Alabama at Birmingham) were eligible for the study. The study population for this periodontal disease supplement to Perinatal Emphasis Research Center was a sample of convenience, in that women were recruited only when delivered during daytime business hours on weekdays. Spontaneous preterm birth was defined as delivery following spontaneous preterm labor or spontaneous preterm premature rupture of membranes. Indicated preterm birth was defined as delivery for maternal or fetal indications excluding chorioamnionitis. All patients enrolled in this periodontal disease supplement to the Perinatal Emphasis Research Center provided informed consent before participation.

Study participants underwent a dental examination by a periodontist from the School of Dentistry within 72 hours postpartum. Eighteen of the women had a dental examination performed at 24 weeks of gestation as part of the larger Perinatal Emphasis Research Center observational study, and the dental examination was not repeated at the postpartum visit for these women. The dental examination technique used was a modification of the Community Periodontal and Treatment Index, also known in the United States as the Periodontal Screening and Recording Index.19 Briefly, the oral cavity and dentition were divided into 6 standard regions or sextants. At least 6 areas of each tooth were examined using a periodontal probe. The highest score in millimeters for any tooth in each sextant was recorded for probing depth and clinical attachment level. To perform the dental examination, a 0.5-mm diameter probe is slipped between the gingiva and the tooth until resistance is met by the probe. The distance from the cemento-enamel junction and pocket base was defined as attachment loss. Any evidence of gingival inflammation, defined as bleeding on periodontal probing of any tooth, was recorded for each sextant. Periodontal health was defined as no evidence of attachment loss or gingival inflammation. Periodontal disease was defined as 1) gingival inflammation and no attachment loss (gingivitis); 2) 3–5 mm (mild periodontitis); or 3) > 5 mm (severe periodontal disease) in any one sextant. The extent of periodontal disease was classified using an index. This Extent Index describes the proportion of sextants with a threshold attachment level (ie, the Extent 5 Index is the proportion of sextants with an attachment loss of > 5 mm).20 In reporting the index, the denominator is sextants in any group of women, not an individual score for each woman.

At the time of delivery, the placenta and a sample of neonatal umbilical cord blood were collected using aseptic technique, refrigerated, and processed for culture within 12 hours of delivery. Placental culture included swabs and placental tissue for aerobic and anaerobic culture and culture for Mycoplasma species and Ureaplasma urealyticum obtained using aseptic technique. The swabs were taken between the chorion and amnion in 3 separate sites. The placental tissue was taken just beneath the chorion. All placentas were then placed in formalin and underwent histologic examination by a single pathologist. Umbilical cord blood was cultured for Mycoplasma sp and U urealyticum, and the remaining fetal cord serum was aliquoted and stored at −70°C for batched analysis. Interleukin-6 (IL-6) levels in the cord serum were determined by commercially available enzyme-linked immunosorbent assay (ELISA) kits (R&D Systems, Inc, Minneapolis, MN). The lower limit of sensitivity of the assay was 0.7 pg/mL. The intra-assay and interassay coefficients of variation were 2.6% and 4.5%, respectively. Concentrations of cord IL-6 greater than or equal to the 95th percentile for the combined indicated preterm and term control groups of the larger Perinatal Emphasis Research Center study were considered elevated. The periodontists, laboratory personnel, and pathologist were blinded to delivery outcome.

Maternal demographic, intrapartum, delivery, and postpartum information was recorded by a trained obstetric research nurse. Neonatal outcome data through hospital discharge or death was also recorded. Neonatal systemic inflammatory response syndrome was defined as the presence of negative cerebrospinal fluid and blood cultures plus clinically suspected sepsis and/or a band/band plus polymorphonuclear cell ratio of 0.15 or greater. Composite neonatal morbidity was defined as any one or more of the following complications: neonatal systemic inflammatory response syndrome, intraventricular hemorrhage (grades 3 or 4), periventricular leukomalacia, respiratory distress syndrome, bronchopulmonary dysplasia, necrotizing enterocolitis, and/or neonatal death.

Based on prior studies in our pregnant patient population,6 we estimated the baseline rate of severe periodontal disease to be 20%. Using a 2-sided test of significance with an α level of 0.05 and power of 80%, we estimated needing 45 cases and 45 term controls, assuming a 50% exposure rate in cases versus a 20% exposure rate in controls (an odds ratio of 4.0). However, because spontaneous preterm deliveries accounted for two thirds of the preterm births at our institution, we calculated the sample size for the preterm birth groups using a 2:1 ratio of cases to controls. We estimated needing 57 spontaneous cases versus 38 indicated controls for the same comparison as described for the term control group. We therefore attempted to recruit 57 cases of spontaneous preterm birth, 38 indicated preterm controls, and 45 term controls for our study.

Statistical analyses were performed using SAS 8.2 software (SAS Institute, Inc, Cary, NC). Analyses were performed for cases and the 2 separate control groups, not across all 3 groups. Unadjusted odds ratios (ORs) and their 95% confidence intervals (CIs) were calculated separately for spontaneous cases compared with indicated and term controls. For demographic characteristics, groups were compared using χ2 tests or Fisher exact test, where appropriate. Means of continuous variables were compared using Student t test. Distribution of IL-6 between groups was compared using a Wilcoxon rank sum test. Logistic regression analysis, adjusting for possible confounding factors, was used to calculate adjusted ORs for spontaneous preterm birth.

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RESULTS

From October 1998 through May 2001, 139 maternal-infant pairs were enrolled: 59 following a spontaneous preterm birth, 36 following an indicated preterm birth, and 44 following uncomplicated spontaneous labor at term. The indicated preterm births included 31 (86%) for severe preeclampsia and 5 (14%) for nonreassuring fetal status. There were no significant differences in birth group among the 18 women with a periodontal examination at 24 weeks (n = 10 term, n = 6 spontaneous preterm, n = 2 indicated preterm; P = .053). Selected maternal demographics are presented in Table 1. Most of the differences noted among the birth groups reflect the demographics of our patient population. Our local patient population (those receiving prenatal care and delivering in our hospital) is predominantly African American, funded by Medicaid, and younger, whereas maternal transfers (from across the state with an expectant preterm delivery) are more likely to be older, have private insurance, and a higher percentage of white women.

Table 1
Table 1
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We evaluated the potential association between periodontal disease and spontaneous preterm birth in several ways. The extent or the number of regions (sextants) with mild-to-severe attachment loss is reported using the Extent Index.20 With a threshold attachment loss of more than 3 mm and more than 5 mm, the Extent 3 and 5 Index for each study group are presented in Table 2. Using either threshold for periodontal disease, the spontaneous preterm birth group had significantly more extensive periodontal disease than the term birth group, ie, more areas of the mouth were affected. The spontaneous preterm birth group also had more extensive periodontal disease than the indicated preterm birth group, but the more than 5 mm threshold was not statistically significant.

Table 2
Table 2
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We also evaluated whether women had evidence of severe disease in at least one area of the mouth in relation to birth group. None of the women had completely healthy gums. Women with a spontaneous preterm birth at less than 32 weeks of gestation had higher rates of severe periodontal disease than both the indicated preterm birth or term birth groups (Table 3). Multivariable analyses were performed, controlling for maternal age, race, education, insurance status, parity, history of a spontaneous preterm birth, and smoking. The unadjusted and adjusted ORs for spontaneous preterm birth in women with periodontal disease compared with women without severe periodontal disease are presented in Table 4. Each regression model included the spontaneous preterm birth group as well as one or both of the control groups. Severe periodontal disease was associated with an almost 3-fold risk for spontaneous preterm birth compared with the combined controls, indicated preterm birth, and term birth (OR 2.6, 95% CI 1.1–6.2). Because periodontal disease may be in the causal pathway in each of a woman's pregnancies, we repeated the logistic regression adjusting for the same factors but excluding history of preterm birth. Again, severe periodontal disease was associated with a 3-fold risk for spontaneous preterm birth (OR 3.4, 95% CI 1.5–7.7; Table 4).

Table 3
Table 3
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Table 4
Table 4
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The association between markers of upper genital tract inflammation at the time of delivery and periodontal disease is presented in Table 5. Women with and without severe periodontal disease had similar rates of positive placental cultures, positive umbilical cord cultures for U urealyticum and Mycoplasma species, histologic chorioamnionitis, funisitis, median cord IL-6 level, and an elevated umbilical cord IL-6 level (≥ 95% or 41.2 pg/mL). These findings were true in the overall population as well as within each birth group (Table 5, data for indicated preterm and term birth not shown). Using the number of participants in the overall population with and without periodontal disease (n = 51 and n = 88, respectively), we determined that we had 80% power (α = 0.05) to detect a significant difference between groups (baseline rate of histological chorioamnionitis of 50% in the group with periodontal disease, compared with 25% in the group without periodontal disease). Organisms that are known periodontal pathogens were identified by placental culture in only 5 of the women (2 women with spontaneous preterm birth and 3 women with a term birth) and included Peptostreptococcus micros, Streptococcus constellatus, and Eubacterium species.21

Table 5
Table 5
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None of the infants delivered at term had any of the adverse neonatal outcomes assessed in this study. Neonatal outcome and presence or absence of severe periodontal disease in the preterm population (spontaneous and indicated) are presented in Table 6. All of the adverse neonatal outcomes evaluated were represented similarly among women with and without periodontal disease.

Table 6
Table 6
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DISCUSSION

The results of our study demonstrate an association between severe periodontal disease and spontaneous preterm birth at less than 32 weeks of gestation. Others have shown an association between periodontal disease and preterm birth.6–8,12–16 In a case-control study of 124 women, Offenbacher and colleagues12 found that preterm low birth weight cases had significantly worse periodontal disease than control women with normal birth weight infants. Cases were defined as women with a current or previous history of a birth in which the infant (< 2,500 g) was delivered after preterm labor or premature rupture of membranes. In their multivariable analysis in that study, the OR for periodontal disease in cases was 7.5 (95% CI 1.95–28.8). These investigators also demonstrated a significant association between periodontal disease and preterm birth in a larger prospective study (n = 814) in which 9% of women delivering at less than 37 weeks and 13.6% of women at less than 32 weeks of gestation had moderate-severe periodontal disease, compared with 4.5% of women delivering at term.8 In a large prospective cohort study of 1,313 women at our institution, Jeffcoat and colleagues6 showed that women with severe periodontal disease at 21–24 weeks of gestation had a higher OR for subsequent spontaneous preterm birth at less than 37 weeks (adjusted OR 4.5, 95% CI 2.2–9.2) and less than 32 weeks of gestation (adjusted OR 7.1, 95% CI 1.7–27.4). Our results are consistent with these findings, with the added strength of comparing well-defined cases of spontaneous preterm birth at less than 32 weeks of gestation and 2 control groups: one of preterm birth following maternal or fetal indications and one of term birth.

The mechanisms by which periodontal disease and preterm birth are associated are not clear. It has been hypothesized that, in the presence of severe periodontal disease, cytokines produced by the infected periodontium may appear in the systemic circulation and target the placenta and fetus, precipitating preterm labor. Alternatively, oral organisms can disseminate hematogenously to target the placenta, membranes, and fetus. This infectious challenge may result in increased cytokine expression and precipitate preterm labor.17–18 In the prospective study by Offenbacher and colleagues8 described above, maternal immunoglobulin (Ig)G and fetal IgM directed against known periodontal pathogens were measured at the time of delivery.22 The highest risk for preterm birth was observed among mothers without evidence of a protective IgG response combined with a fetus with an IgM response (OR 10.3, P < .001).22 These data would suggest that when the fetal-placental unit is exposed to the periodontal pathogens in the absence of maternal antibody protection, this may precipitate preterm birth.

Previous reports have documented a consistent relationship between upper genital tract infection/inflammation and preterm birth, particularly early spontaneous preterm birth.3–5 Previous studies have not evaluated the presence of upper genital tract inflammation at the time of delivery and the potential association with periodontal disease. In our study, we could not demonstrate any association between markers of upper genital tract inflammation at the time of birth and moderate-to-severe periodontal disease in cases of spontaneous preterm birth, indicated preterm birth, or term controls. Our data would suggest that the potential mechanism of periodontal disease–associated preterm birth is not hematogenous spread of the periodontal organisms to the placenta with colonization and subsequent inflammation precipitating preterm labor or premature rupture of membranes.

Periodontal pathogenic organisms may be more difficult to culture from the placenta. However, we used meticulous methods and were able to isolate multiple species of anaerobic and Gram-negative organisms, including several known periodontal pathogens. Perhaps the relative lack of growth of periodontal organisms represents sampling error. However, we sampled multiple sites of the chorioamnion, as well as placental tissue, for culture in these women. It is possible that the organisms do spread to the placenta but are not viable and do not colonize the placenta and membranes. Perhaps more sensitive tests, such as DNA tests for periodontal pathogens, may demonstrate that the presence of the organisms and the antigenic challenge of these few bacteria is enough to precipitate preterm labor. Regardless, the inflammation that occurs is not sufficient to be demonstrated by evidence of higher rates of histological chorioamnionitis or elevated umbilical cord levels of the proinflammatory cytokine, IL-6. Another possibility to consider is that periodontal disease and spontaneous preterm birth are not, in fact, directly associated in a cause-and-effect manner. Rather, these 2 conditions may be linked by a third factor that predisposes the pregnant woman to both adverse outcomes: periodontal disease and spontaneous preterm birth.

Finally, previous studies of inflammation and preterm birth have demonstrated an increased risk for neonatal morbidity, especially neurological morbidity, in the setting of intrauterine infection and inflammation.23–28 We did not see an association between periodontal disease and adverse neonatal outcome in the preterm infants in our study. This further suggests that, if the preterm birth associated with periodontal disease is inflammation-mediated, the levels of inflammation are not of the same magnitude as those seen in infection-mediated preterm birth previously studied. Further investigation into the potential etiology of the association between periodontal disease and preterm birth is warranted.

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REFERENCES

1. Hack M, Fanaroff AA. Outcomes of children of extremely low birthweight and gestational age in the 1990s. Semin Neonatol 2000;5:89–106.

2. Martin JA, Hamilton BE, Sutton PD, Ventura SJ, Menacker F, Munson ML. Births: final data for 2002. Natl Vital Stat Rep. 2003;52(10):1–16.

3. Andrews WW, Goldenberg RL, Hauth JC. Preterm labor: emerging role of genital tract infections. Infect Agents Dis 1995;4:196–211.

4. Hauth JC, Andrews WW, Goldenberg RL. Infection-related risk factors predictive of spontaneous preterm birth. Prenat Neonat Med 1998;3:86–9.

5. Goldenberg RL, Hauth JC, Andrews WW. Intrauterine infection and preterm delivery. N Engl J Med 2000;342:1500–7.

6. Jeffcoat MK, Geurs NC, Reddy MS, Cliver SP, Goldenberg RL, Hauth JC. Periodontal infection and preterm birth: results of a prospective study. J Am Dent Assoc 2001;132:875–80.

7. Jeffcoat MK, Geurs NC, Reddy MS, Goldenberg RL, Hauth JC. Current evidence regarding periodontal disease as a risk factor in preterm birth. Ann Periodontol 2001;6:183–8.

8. Offenbacher S, Lieff S, Boggess K, Murtha AP, Madianos PN, Champagne CM, et al. Maternal periodontitis and prematurity. Part I: Obstetric outcome of prematurity and growth restriction. Ann Periodontol 2001;6:164–74.

9. Offenbacher S, Beck JD, Lieff S, Slade G. Role of periodontitis in systemic health: spontaneous preterm birth. J Dent Educ 1998;62:852–8.

10. Zeeman GG, Veth EO, Dennison DK. Focus on primary care: periodontal disease: implications for women's health. Obstet Gynecol Surv 2001;56:43–9.

11. Teng YT, Taylor GW, Scannapieco F, Kinane DF, Curtis M, Beck JD, et al. Periodontal health and systemic disorders. J Can Dent Assoc 2002;68:188–92.

12. Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, et al. Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontal 1996;67:1103–13.

13. Jeffcoat MK, Hauth JC, Geurs NC, Reddy MS, Cliver SP, Hodkins PM, et al. Periodontal disease and preterm birth: results of an intervention study. J Periodontol 2003;74:1214–8.

14. Lopez NJ, Smith PC, Gutierrez J. Periodontal therapy may reduce the risk of preterm low birth weight in women with periodontal disease: a randomized controlled trial. J Periodontol 2002;73:911–24.

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

16. Dasanayake AP, Russell S, Boyd D, Madianos PN, Forster T, Hill E. Preterm low birth weight and periodontal disease among African-Americans. Dent Clin North Am 2003;47:115–25.

17. 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.

18. Bearfield C, Davenport ES, Sivapathasundaram V, Allaker RP. Possible association between amniotic fluid micro-organism infection and microflora in the mouth. BJOG 2002;109:527–33.

19. Cutress TW, Ainamo J, Sardo-Infirri J. The community periodontal index of treatment needs (CPTIN) procedure for population groups and individuals. Int Dent J 1987;37:222–33.

20. Carlos J, Wolfe M, Kingman A. The extent and severity index: a simple method for use in epidemiologic studies of periodontal disease. J Clin Periodontol 1986;13:500–5.

21. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998;25:134–44.

22. Madianos PN, Lieff S, Murtha AP, Boggess KA, Auten RL Jr, Beck JD, et al. Maternal periodontitis and prematurity. Part 2: Maternal infection and fetal exposure. Ann Periodontol 2001;6:175–82.

23. Alexander JM, Gilstrap LC, Cox SM, McIntire DM, Leveno KJ. Clinical chorioamnionitis and the prognosis for very low birth weight infants. Obstet Gynecol 1998;91:725–9.

24. Wu YW, Colford JM Jr. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. JAMA 2000;284:1417–24.

25. Yoon BH, Jun JK, Romero R, Park KH, Gomez R, Choi JH, et al. Amniotic fluid inflammatory cytokines (interleukin-6, interleukin-1β, and tumor necrosis factor-α), neonatal brain white matter lesions, and cerebral palsy. Am J Obstet Gynecol 1997;177:19–26.

26. Yoon BH, Romero R, Park JS, Kim CJ, Kim SH, Choi JH, et al. Fetal exposure to an intra-amniotic inflammation and the development of cerebral palsy at age three years. Am J Obstet Gynecol 2000;182:675–81.

27. Yoon BH, Romero R, Yang SH, Jun JK, Kim IO, Choi JH, et al. Interleukin-6 concentrations in umbilical cord plasma are elevated in neonates with white matter lesions associated with periventricular leukomalacia. Am J Obstet Gynecol 1996;174:1433–40.

28. Dammann O, Leviton A. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 1997;42:1–8.

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Fertility and Sterility, 91(2): 335-342.
10.1016/j.fertnstert.2007.12.075
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
Journal of Clinical Periodontology
Women with a recent history of early-onset pre-eclampsia have a worse periodontal condition
Kunnen, A; Blaauw, J; van Doormaal, JJ; van Pampus, MG; van der Schans, CP; Aarnoudse, JG; van Winkelhoff, AJ; Abbas, F
Journal of Clinical Periodontology, 34(3): 202-207.
10.1111/j.1600-051X.2006.01036.x
CrossRef
Journal of Perinatal Medicine
The relationship between periodontal disease, bacterial vaginosis, and preterm birth
Pretorius, C; Jagatt, A; Lamont, RF
Journal of Perinatal Medicine, 35(2): 93-99.
10.1515/JPM.2007.039
CrossRef
Neuroendocrinology Letters
Relationship of vaginal microflora to PROM, pPROM and the risk of early-onset neonatal sepsis
Veleminsky, M; Tosner, J
Neuroendocrinology Letters, 29(2): 205-221.

Journal of Health Care for the Poor and Underserved
CenteringPregnancySmiles (TM): Implementation of a Small Group Prenatal Care Model with Oral Health
Skelton, J; Mullins, R; Langston, LT; Womack, S; Ebersole, JL; Rising, SS; Kovarik, R
Journal of Health Care for the Poor and Underserved, 20(2): 545-553.

American Journal of Reproductive Immunology
Activation of the Alternative Pathway of Complement is a Feature of Pre-Term Parturition but not of Spontaneous Labor at Term
Vaisbuch, E; Romero, R; Erez, O; Mazaki-Tovi, S; Kusanovic, JP; Soto, E; Dong, Z; Chaiworapongsa, T; Kim, SK; Ogge, G; Pacora, P; Yeo, L; Hassan, SS
American Journal of Reproductive Immunology, 63(4): 318-330.
10.1111/j.1600-0897.2009.00800.x
CrossRef
New England Journal of Medicine
Preterm birth and periodontal disease
Goldenberg, RL; Culhane, JF
New England Journal of Medicine, 355(): 1925-1927.

Bjog-An International Journal of Obstetrics and Gynaecology
The preterm parturition syndrome
Romero, R; Espinoza, J; Kusanovic, JP; Gotsch, F; Hassan, S; Erez, O; Chaiworapongsa, T; Mazor, M
Bjog-An International Journal of Obstetrics and Gynaecology, 113(): 17-42.
10.1111/j.1471-0528.2006.01120.x
CrossRef
American Journal of Obstetrics and Gynecology
Periodontal disease and adverse birth outcomes: a study from Pakistan
Mobeen, N; Jehan, I; Banday, N; Moore, J; McClure, EM; Pasha, O; Wright, LL; Goldenberg, RL
American Journal of Obstetrics and Gynecology, 198(5): -.
ARTN 514.e1
CrossRef
Journal of Reproductive Immunology
Inflammatory processes in preterm and term parturition
Christiaens, I; Zaragoza, DB; Guilbert, L; Robertson, SA; Mitchell, BF; Olson, DM
Journal of Reproductive Immunology, 79(1): 50-57.
10.1016/j.jri.2008.04.002
CrossRef
American Journal of Physical Anthropology
Oral Health and Frailty in the Medieval English Cemetery of St Mary Graces
DeWitte, SN; Bekvalac, J
American Journal of Physical Anthropology, 143(3): 341-354.
10.1002/ajpa.21228
CrossRef
Journal of the American Dental Association
The National Institute of Dental and Craniofacial Research - Research for the practicing dentist
Pihlstrom, BL; Tabak, L
Journal of the American Dental Association, 136(6): 728-737.

Lancet
Periodontal diseases
Pihlstrom, BL; Michalowicz, BS; Johnson, NW
Lancet, 366(): 1809-1820.

Health Technology Assessment
Screening to prevent spontaneous preterm birth: systematic reviews of accuracy and effectiveness literature with economic modelling
Honest, H; Forbes, CA; Duree, KH; Norman, G; Duffy, SB; Tsourapas, A; Roberts, TE; Barton, PM; Jowett, SM; Hyde, CJ; Khan, KS
Health Technology Assessment, 13(): 1-+.
10.3310/hta13430
CrossRef
American Journal of Public Health
Addressing health care disparities and increasing workforce diversity: The next step for the dental, medical, and public health professions
Mitchell, DA; Lassiter, SL
American Journal of Public Health, 96(): 2093-2097.
10.2105/AJPH.2005.082818
CrossRef
Clinics in Perinatology
Pathophysiology of preterm birth: Emerging concepts of maternal infection
Boggess, KA
Clinics in Perinatology, 32(3): 561-+.
10.1016/j.clp.2005.05.002
CrossRef
American Journal of Obstetrics and Gynecology
Treatment of localized periodontal disease in pregnancy does not reduce the occurrence of preterm birth: results from the Periodontal Infections and Prematurity Study (PIPS)
Macones, GA; Parry, S; Nelson, DB; Strauss, JF; Ludmir, J; Cohen, AW; Stamilio, DM; Appleby, D; Clothier, B; Sammel, MD; Jeffcoat, M
American Journal of Obstetrics and Gynecology, 202(2): -.
ARTN 147.e1
CrossRef
Journal of Womens Health
Maternal Serum Granulocyte Colony-Stimulating Factor Levels and Spontaneous Preterm Birth
Whitcomb, BW; Schisterman, EF; Luo, XP; Chegini, N
Journal of Womens Health, 18(1): 73-78.
10.1089/jwh.2008.0883
CrossRef
Periodontology 2000
Maternal periodontal disease and spontaneous preterm birth
Michalowicz, BS; Durand, R
Periodontology 2000, 44(): 103-112.

Journal of the American Dental Association
Exploring the relationship between periodontal disease and pregnancy complications
Bobetsis, YA; Barros, SP; Offenbacher, S
Journal of the American Dental Association, 137(): 7S-13S.

American Journal of Obstetrics and Gynecology
Fetal immune response to oral pathogens and risk of preterm birth
Boggess, KA; Moss, K; Madianos, P; Murtha, AP; Beck, J; Offenbacher, S
American Journal of Obstetrics and Gynecology, 193(3): 1121-1126.
10.1016/j.ajog.2005.05.050
CrossRef
Journal of Maternal-Fetal & Neonatal Medicine
Maternal plasma visfatin in preterm labor
Mazaki-Tovi, S; Romero, R; Vaisbuch, E; Erez, O; Chaiworapongsa, T; Mittal, P; Kim, SK; Pacora, P; Gotsch, F; Dong, Z; Hassan, SS; Kusanovic, JP
Journal of Maternal-Fetal & Neonatal Medicine, 22(8): 693-704.
10.1080/14767050902994788
CrossRef
Bjog-An International Journal of Obstetrics and Gynaecology
Periodontal disease and adverse pregnancy outcomes: a systematic review
Xiong, X; Buekens, P; Fraser, WD; Beck, J; Offenbacher, S
Bjog-An International Journal of Obstetrics and Gynaecology, 113(2): 135-143.
10.1111/j.1471-0528.2005.00827.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
Biomedical Research-Tokyo
Vascular endothelial growth factor induces mRNA expression of pro-inflammatory factors in the uterine cervix of mice
Nguyen, BTA; Minkiewicz, V; McCabe, E; Cecile, J; Mowa, CN
Biomedical Research-Tokyo, 33(6): 363-372.

Plos One
The SEPS1 G-105A Polymorphism Is Associated with Risk of Spontaneous Preterm Birth in a Chinese Population
Wang, Y; Yang, X; Zheng, Y; Wu, ZH; Zhang, XA; Li, QP; He, XY; Wang, CZ; Feng, ZC
Plos One, 8(6): -.
ARTN e65657
CrossRef
Archives of Gynecology and Obstetrics
Can leukocyte count during the first trimester of pregnancy predict later gestational complications?
Tzur, T; Weintraub, AY; Sergienko, R; Sheiner, E
Archives of Gynecology and Obstetrics, 287(3): 421-427.
10.1007/s00404-012-2603-0
CrossRef
Iranian Journal of Reproductive Medicine
Association between preterm and low-birth weight with periodontal disease: a case-control study
Khadem, N; Rahmani, ME; Sanaei, A; Afiat, M
Iranian Journal of Reproductive Medicine, 10(6): 561-566.

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
Obstetrics & Gynecology
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.
10.1097/01.AOG.0000190212.87012.96
PDF (242) | CrossRef
Obstetrical & Gynecological Survey
Periodontal Disease and Pregnancy Outcomes: State-of-the-Science
Xiong, X; Buekens, P; Vastardis, S; Yu, SM
Obstetrical & Gynecological Survey, 62(9): 605-615.
10.1097/01.ogx.0000279292.63435.40
PDF (590) | CrossRef
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Associations of periodontitis and oral manifestations with CD4 counts in human immunodeficiency virus-pregnant women in Thailand
Pattrapornnan, P; DeRouen, TA
Oral Surgery Oral Medicine Oral Pathology Oral Radiology, 116(3): 306-312.
10.1016/j.oooo.2013.04.016
CrossRef
Journal of Periodontology
Effects of periodontal therapy during pregnancy on periodontal status, biologic parameters, and pregnancy outcomes: A pilot study
Offenbacher, S; Lin, DM; Strauss, R; McKaig, R; Irving, J; Barros, SP; Moss, K; Barrow, DA; Hefti, A; Beck, JD
Journal of Periodontology, 77(): 2011-2024.
10.1092/jop.2006.060047
CrossRef
Journal of Public Health Dentistry
Periodontitis and gestational diabetes mellitus: Exploring the link in NHANES III
Novak, KF; Taylor, GW; Dawson, DR; Ferguson, JE; Novak, MJ
Journal of Public Health Dentistry, 66(3): 163-168.

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