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Clinical

The Relationship between Periodontitis and Preterm Low Birthweight

M.V. Vettore1,2,*, M. doC. Leal1, A.T. Leão3, A.M. Monteiro da Silva4, G.A. Lamarca5 and A. Sheiham2

1 Department of Epidemiology and Quantitative Methods in Health, Oswaldo Cruz Foundation (ENSP/FIOCRUZ), Rua Leopoldo Bulhões, 1480-Manguinhos, 8° andar, Rio de Janeiro, CEP 21041-210 RJ, Brazil;
2 Department of Epidemiology and Public Health, University College London Medical School, London, UK;
3 Graduate Periodontics, School of Dentistry, Federal University of Rio de Janeiro (UFRJ), RJ, Brazil;
4 Institute of Human and Social Sciences, Rural Federal University of Rio de Janeiro (UFRRJ), RJ, Brazil; and
5 Section of Periodontology, Brazilian Dental Association, Petropolis, Brazil

Correspondence: * corresponding author, mario{at}ensp.fiocruz.br


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PARTICIPANTS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
There is no consensus about the influence of periodontal disease on preterm low birthweight. The objective was to investigate the relationship between periodontal disease and preterm low birthweight. A case-control study with 542 post partum women aged over 30 yrs was conducted. Three groups of cases were compared with non-preterm and non-low-birthweight control individuals (n = 393): low birthweight (n = 96), preterm (n = 110), and preterm and low birthweight (n = 63). Periodontal clinical parameters and covariates were recorded. Periodontal disease levels were higher in control individuals than in cases. The extent of periodontal disease did not increase risk of preterm low birthweight according to 15 measures of periodontal disease. Mean periodontal pocket depth and frequency of periodontal sites with clinical attachment level ≥ 3 mm in preterm low birthweight cases were lower than in control individuals. Periodontal disease was not more severe in women with preterm low birthweight babies.

Key Words: periodontal disease • preterm • low birthweight • case-control • risk factors


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PARTICIPANTS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Preterm low birthweight is an important cause of morbidity and mortality in newborns in Latin America. Despite intensive research on the etiology of preterm low birthweight, in over 50% of clinical cases, the cause remains unknown (Barros et al., 1992).

It has been claimed that periodontal infection increases the risk of preterm low birthweight. Early evidence has shown that women delivering preterm low birthweight babies were almost 8 times more likely to have periodontal disease (Offenbacher et al., 1996). The "Focal Infection Theory" proposed by Hunter in 1910 was being resurrected. According to Hunter’s theory, bacteria and their products from local infections could be disseminated throughout the body and cause diseases in other organs (Billings, 1912).

Offenbacher and co-workers’ study was followed by others. Most claimed a positive relationship (Dasanayake et al., 2001; Jeffcoat et al., 2001; Offenbacher et al., 2001). In contrast, Davenport and coworkers (2002) reported no association, and a systematic review reported limited evidence that periodontitis is associated with increased risk for preterm low birthweight (Madianos et al., 2002). A later systematic review highlighted that most studies on the subject had serious methodological limitations that could lead to spurious conclusions (Vettore et al., 2006).

The uncertainties on the relationship between periodontal infection and risks for preterm low birthweight prompted us to carry out a methodologically robust case-control study to test the hypothesis. The objective of this study was to investigate the relationship between clinical parameters of periodontal disease and preterm low birthweight in women over 30 yrs old.


   PARTICIPANTS & METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PARTICIPANTS & METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
A case-control study was conducted based on primary and secondary data gathered from 4 public maternity hospitals in Rio de Janeiro, Brazil. The maternity units are referral centers for high-risk pregnancies. Three definitions of cases were considered: Low birthweight, Preterm birth, and Preterm birth and low birthweight. All case groups were compared with a control group of non-preterm birth and non-low-birthweight mothers. The study was approved by the Committee of Ethics and Research of the National School of Public Health-Oswaldo Cruz Foundation (protocol no. 78/02).

Assuming a 15% periodontal disease prevalence among control individuals and 25% among cases, with 80% power and 5% Type I error probability, a study with a selection ratio case/control of 3:1 required 551 participants (Flores-de-Jacoby et al., 1991).

We conducted a pilot study to adapt and test questionnaires. Examiner calibration for periodontal clinical parameters was performed. Kappa test and Intra-class Correlation Coefficient of agreement for periodontal pocket depth were, respectively, ≥0.78 and ≥ 0.72 for intra-examiner, and ≥ 0.77 and ≥ 0.72 for inter-examiner. All examiners were masked concerning the purpose of the study.

We recruited 542 eligible women for the study, achieving 79% power. Data were obtained from structured interviews, medical records, and periodontal clinical examinations conducted by six examiners. Inclusion and exclusion criteria are provided in Appendix 1.

Babies delivered before 37 complete wks of gestation were considered as preterm (PB). Estimation of gestational age was assessed from the last menstrual period (Berg, 1991). When last menstrual period data were missing, we used the Capurro score to estimate gestational age (Capurro et al., 1978). Intraclass Correlation Coeficient between last menstrual period and Capurro score was 0.92. Low-birthweight newborns were infants weighing less than 2500 g at birth. All newborns were weighed immediately after delivery, with calibrated scales. Gestational age and infant weights were obtained from medical records.

Periodontal clinical measurements included Visible Plaque Index (Ainamo and Bay, 1975), visible calculus, Bleeding on Probing Index (Ainamo and Bay, 1975), Periodontal Pocket Depth, and Clinical Attachment Level measured at 6 sites per tooth (mesiobuccal, buccal, distobuccal, distolingual, lingual, and mesiolingual) for all teeth, excluding third molars.

Periodontal pocket depth and clinical attachment level measures were recorded to the nearest higher millimeter by means of the North Carolina periodontal probe (Hu-Friedy®, Chicago, IL, USA), 15 mm in length and 0.35 mm in diameter. Oral plain mirrors (Hu-Friedy®) and a head light (model 8720, Trilhas & Rumos®, Teresópolis, Brazil) were used to facilitate periodontal examinations. The average time interval between delivery and periodontal examination was approximately 1 day.

Covariate data were collected from medical records or through structured interviews. Anthropometric and socio-demographic characteristics included height, Body Mass Index, ethnicity, education level, marital status, and information on work and income. The overall level of housing conditions was assessed based on 14 characteristics of housing. The women were questioned concerning smoking and alcohol intake, before and during pregnancy. CAGE (Ewing, 1984) and T-ACE (Sokol et al., 1989) questionnaires were used to detect alcoholism and risky drinking, respectively. The women answered questions about illicit drug use, physical violence, contraceptive methods, and parental desire for and satisfaction with pregnancy. Physical activities during the gestational period were assessed by an EPAL questionnaire (Vasconcelos and Anjos, 2003). Anxiety and depression were assessed through validated Brazilian versions of the Spielberger Trait Anxiety Inventory (Spielberger et al., 1970) and The Minnesota Multiphasic Personality Inventory (Hathaway and McKinley, 1943).

Pregnancy information—including gestational age, baby weight at birth, type of birth, sex of neonate, baby length, and proportion weight/gestational age—was transcribed from medical records. Occurrences of hypertension, pre-eclampsia, hepatitis B, anemia, gestational diabetes, urinary infection, and infections during pregnancy were also recorded. Prenatal care attendance was assessed by the modified Kotelchuck index (Leal et al., 2004). (A detailed description of methods is in APPENDIX 1.)

Statistical Analysis
All statistical analyses were carried out with SPSS 10.0 (Statistical Package for the Social Sciences for Windows®, SPSS Inc., Chicago, IL, USA) with a significance level of 5% (p ≤ 0.05).

Periodontal Clinical Parameters
Clinical parameters—including number and percentage of sites with visible plaque and calculus, bleeding on probing, and average of periodontal pocket depth and clinical attachment levels—were computed for each person and then averaged across participants in the groups. Differences among clinical parameters were examined in the subset of sites according to their periodontal pocket depth (≥ 4 mm, ≥5 mm, and ≥ 6 mm), clinical attachment level (≥3 mm, ≥4 mm, ≥5 mm, and ≥ 6 mm), and a combination of both (periodontal pocket depth ≥ 4 mm and clinical attachment level ≥ 3 mm). The statistical significance of differences between and among groups was checked by Mann-Whitney tests.

Thirteen different definitions for periodontal disease, based on previously published studies on this subject, were used (Fig. 2Go). In addition, the sample was divided into different quartiles of frequency distribution, according to the number of periodontal pockets with depth ≥ 4 mm and the sum of all periodontal pockets with depth ≥ 4 mm in sites with clinical attachment level ≥ 4 mm, referred to as Periodontal Inflammatory Load. Quartiles of distribution of periodontal pockets with depth ≥ 4 mm and Periodontal Inflammatory Load were calculated and participants grouped in 4 different levels of periodontal pocket depth and Periodontal Inflammatory Load. In both strategies, Mantel-Haenszel Odds Ratios were calculated, with Level 1 as the category of reference.


Figure 2
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  		Figure 2. Unadjusted odds ratios between periodontal disease in preterm low-birthweight mothers and control individuals. [CI: confidence interval (95%); Odds ratio could not be performed]

 
Covariates
Covariate variables were computed for each participant and then each group. Comparisons between and among groups were tested by the Chi-square test and Fisher’s Exact test for variables expressed in proportions, and by the Mann-Whitney test and t test for continuous variables. Internal consistencies for depression and anxiety scales were evaluated by Cronbach’s a coefficient.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PARTICIPANTS & METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Of 2561 puerperal women invited, 172 (6.7%) declined to participate in the study. Of the 2389 who agreed, 1847 were excluded for different reasons, resulting in 542 selected participants (Fig. 1Go). Gestational age and newborn weight at birth were available in 98% and 100% of medical records, respectively. The sample of preterm mothers included 110 persons, and there were 96 low-birthweight cases.


Figure 1
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  		Figure 1. Flow chart for selection of study participants.

 
Gestational age at birth and birthweight were significantly lower in all case groups (Table 1Go). There were no differences in type of birth, neonate’s sex, mother’s age, ethnicity, alcohol consumption, depression, and urinary infection between and among groups (Table 1Go). Body Mass Index was significantly lower in preterm low-birthweight cases, compared with control groups, and there were slightly more married women in the control groups. The low-birthweight group tended to have a higher proportion of women who smoked during pregnancy. Numbers of cigarettes smoked per day were more in preterm low-birthweight mothers. Trait anxiety scores were significantly associated with low birthweight and with preterm. All cases were more likely to have had previous preterm and low-birthweight babies. Inadequate prenatal care was more common in low-birthweight, preterm, and preterm and low-birthweight individuals (P < 0.005). Frequency of gestational hypertension was higher in preterm, preterm and low-birthweight, than in control individuals (Table 1Go). Pre-eclampsia was not more common in mothers having preterm and low-birthweight babies. There was a borderline association between gestational diabetes and preterm births. (A more detailed description of all covariates is in APPENDIX 2 and APPENDIX Tables 1, 2, 3, and 4.)


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  		Table 1. Covariate Variables of the 542 Women Examined in the Study
 
Number of teeth, bleeding on probing, and level of calculus were similar in all pairs of cases and control groups, whereas the Visible Dental Plaque scores were significantly higher in control individuals compared with preterm cases (P = 0.042) (Table 2Go).


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  		Table 2. Periodontal Clinical Parameters in the Case-Control Groups
 
Mean periodontal pocket depth and clinical attachment level, mean and frequency of periodontal pocket depth ≥ 4 mm, clinical attachment level ≥ 3 mm, and periodontal pocket depth ≥ 4 mm with clinical attachment level ≥ 3 mm were significantly higher in control individuals compared with those in the low-birthweight group (P ≤ 0.05) (Table 2Go). Mean periodontal pocket depth and mean and frequency of clinical attachment level ≥ 3 mm were lower in women with preterm births. Periodontal pocket depth and clinical attachment level mean and mean and frequency of clinical attachment level ≥ 3 mm were significantly lower in women with preterm births and low-birthweight babies (Table 2Go).

Unadjusted risk estimates [odds ratio (OR)] were calculated between periodontal disease and preterm low-birthweight outcomes. Periodontitis was more prevalent in control individuals compared with preterm low-birthweight cases by all 13 methods of defining the extent of periodontal disease (Fig. 2Go). Frequency of periodontal sites with periodontal pocket depth ≥ 4 mm in women with low birthweight, preterm, and preterm and low birthweight was not higher than in control individuals. Case individuals tended to have less Periodontal Inflammatory Load than control individuals (Fig. 2Go).


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PARTICIPANTS & METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The hypothesis that periodontal disease is a risk factor for undesirable pregnancy outcomes was rejected. Unlike some studies on the subject, clinical measures relating to periodontal disease were not associated with low birthweight, preterm, and preterm and low birthweight. Furthermore, control individuals had significantly more severe clinical periodontal disease.

There is no consensus on a uniform definition of periodontal disease in studies on periodontal disease and preterm low birthweight (Madianos et al., 2002; Vettore et al., 2006). To overcome that, we used all 13 measures of periodontal disease used by workers in this research field.

For all 13 measures, woman having preterm low-birthweight babies had less periodontal disease than did control individuals. Therefore, multivariate analyses were not performed. Case definition numbers 14 and 15 facilitated the assessment of a possible dose-response relationship between severity of destructive periodontal disease and pregnancy outcomes. There was a steady decrease in estimates of association between periodontal disease and preterm low birthweight among groups with more destructive periodontal disease. This finding provides strong evidence of no association between periodontal disease and pregnancy outcomes, since the dose-response relationship is an important test in epidemiological studies identifying new causal factors.

It is interesting to note that, in 5 of the periodontal disease criteria, periodontal disease was protective in the unadjusted analysis. Although this protective effect might disappear in adjusted analysis, future studies should investigate possible effects of the underlying inflammation-related cascade of events caused by periodontal disease on the placental region.

The finding that periodontal clinical parameters in cases were not higher than in control individuals is in accord with results from some previous studies associating periodontal disease and preterm low birthweight (Mitchell-Lewis et al., 2001; Moore et al., 2004). In addition, evidence of no association between periodontal disease and preterm low birthweight in this study was also reported by others (Davenport et al., 2002; Lunardelli and Peres, 2005; Rajapakse et al., 2005; Michalowicz et al., 2006).

Heterogeneity in diagnostic criteria for periodontal disease in previous studies is an important source of discrepancies (Vettore et al., 2006). The strength of our study is that a wide range of measures of periodontal disease was used to avoid objections about measuring periodontal disease. Approaches included all methods used previously. In contrast to our findings, several studies found positive associations between periodontal disease and preterm low birthweight (Offenbacher et al., 1996, 2001; Lopez et al., 2002; Radnai et al., 2004; Dörtbudak et al., 2005; Jarjoura et al., 2005; Marin et al., 2005; Moliterno et al., 2005). One possible explanation for their positive findings is poor control for potential confounders. In our study, exclusion selection criteria for participants were relevant confounders, such as chronic diseases like diabetes mellitus and previous periodontal treatment. Exclusion of women with chronic hypertension avoided bias of confounding, since anti-hypertensive medications are strongly related to periodontal status. Women using antibiotics in the week preceding the study were excluded because of effects of antibiotics on periodontal tissues. Antibiotics given in pregnancy are usually for genito-urinary tract infections. This might explain the lack of association between genito-urinary infection and preterm low birthweight in the current study.

Classification bias is the most common systematic error compromising validity of case-control studies. In our study, gestational age was estimated through the last menstrual period, the gold standard method for gestational age assessment in epidemiological studies (Berg, 1991). ‘Last menstrual period’ information was missing in 18% of medical records, and the Capurro score was used to estimate gestational age in such persons, with high agreement of diagnostic reliability. Reliable sources of information for gestational age and weight at birth, obtained from medical records, avoided potential classification bias.

In summary, periodontal disease is not a risk factor for low birthweight, preterm, and preterm and low birthweight.

Case definitions
(1) ≥ 1 site with a periodontal pocket depth ≥ 5 mm in each quadrant, not accounting for the periodontal pocket depth at the distal aspects of the most posterior tooth in the quadrant (Dörtbudak et al., 2005). (2) ≥ 1 site with periodontal pocket depth ≥ 4 mm and ≥ 50% bleeding on probing (Radnai et al., 2004; Lunardelli and Peres, 2005). (3) ≥ 4 sites with periodontal pocket depth ≥ 3.5 mm (Lunardelli and Peres, 2005). (4) Mean periodontal pocket depth, Plaque Index, and bleeding on probing > than the median (Rajapakse et al., 2005). (5) > 3 sites with clinical attachment level ≥ 3 mm (Jeffcoat et al., 2003). (6) ≥ 5 sites with clinical attachment level ≥ 3 mm (Jarjoura et al., 2005). (7) ≥60% sites with clinical attachment level ≥ 3 mm (Offenbacher et al., 1996). (8) ≥ 4 sites with clinical attachment level ≥ 3 mm and periodontal pocket depth ≥ 4 mm (Moliterno et al., 2005). (9) ≥ 4 teeth with ≥ 1 sites with clinical attachment level ≥ 3 mm and periodontal pocket depth ≥ 4 mm in the same site (López et al., 2002). (10) > 5% with periodontal pocket depth ≥ 5 mm and > 5% sites with clinical attachment level ≥ 3 mm (Moore et al., 2004). (11) ≥ 1 site with periodontal pocket depth ≥ 5 mm and ≥ 2 sites with clinical attachment level > 6 mm and bleeding on probing > 5% (Marin et al., 2005). (12) PH (Periodontal health): absence of any periodontal pocket depth > 3 mm and no sites with clinical attachment level > 2 mm. MP (Mild periodontitis): had less disease than the moderate-to-severe group and had more disease than the healthy group. MSP (Moderate-to-severe periodontitis): ≥4 sites with periodontal pocket depth ≥ 5 mm and clinical attachment level ≥ 2 mm (Offenbacher et al., 2001). (13) ND (No disease): < 3 sites with clinical attachment level ≥ 3 mm. P (Periodontitis): ≥ 3 sites with clinical attachment level ≥ 3 mm. GPD (Generalized periodontal disease): ≥ 90 of sites with clinical attachment level ≥ 3 mm (Jeffcoat et al., 2001). (14) Different groups by percentiles of periodontal sites with periodontal pocket depth ≥ 4 mm. Percentiles: P25 = 2, P50 = 11, P75 = 24. Level 1: 0 to 1 sites with periodontal pocket depth ≥ 4 mm. Level 2: 2 to 10 sites with periodontal pocket depth ≥ 4 mm. Level 3: 11 to 23 sites with periodontal pocket depth ≥ 4 mm. Level 4: 24 or more sites with periodontal pocket depth ≥ 4 mm. (15) Different groups by percentiles of sum of all periodontal pocket depths ≥ 4 mm in sites with clinical attachment level ≥ 4 mm (Periodontal Inflammatory Load). Percentiles: P25 = 8, P50 = 47, P75 = 100. Level 1: 0 to 7 mm, the sum of all periodontal pocket depths ≥ 4 mm in sites with clinical attachment level ≥ 4 mm. Level 2: 8 to 46 mm, the sum of all periodontal pocket depths ≥ 4 mm in sites with clinical attachment level ≥ 4 mm. Level 3: 47 to 99 mm, the sum of all periodontal pocket depths ≥ 4 mm in sites with clinical attachment level ≥ 4 mm. Level 4: 100 mm and over, the sum of all periodontal pocket depths ≥ 4 mm in sites with clinical attachment level ≥ 4 mm.


   ACKNOWLEDGMENTS
 
The authors thank Mirella Galvão. This investigation was supported by CNPq, CAPES, FAPERJ Grant E-26/170.421/2003, Hu-friedy do Brasil, and PAHO/WHO.


   FOOTNOTES
 
A supplemental appendix to this article is published electronically only at http://jdr.iadrjournals.org/cgi/content/full/87/1/73/DC1.

Received for publication December 14, 2005. Revision received September 13, 2007. Accepted for publication October 12, 2007.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 PARTICIPANTS & METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

  • Ainamo J, Bay I (1975). Problems and proposals for recording gingivitis and plaque. Int Dent J 25:229–235.[Medline] [Order article via Infotrieve]
  • Barros FC, Huttly SR, Victora CG, Kirkwood BR, Vaughan JP (1992). Comparison of the causes and consequences of prematurity and intrauterine growth retardation: a longitudinal study in southern Brazil. Pediatrics 90:238–244.[Abstract/Free Full Text]
  • Berg A (1991). Menstrual cycle length and the calculation of gestational age. Am J Epidemiol 133:585–589.[Abstract/Free Full Text]
  • Billings F (1912). Chronic focal infections and their etiologic relations to arthritis and nephritis. Arch Intern Med 9:484–498.
  • Capurro H, Konichezky S, Fonseca D, Caldeyro-Barcia R (1978). A simplified method for diagnosis of gestational age in the newborn infant. J Pediatr 93:120–122.[Medline] [Order article via Infotrieve]
  • Dasanayake AP, Boyd D, Madianos PN, Offenbacher S, Hills E (2001). The association between Porphyromonas gingivalis-specific maternal serum IgG and low birth weight. J Periodontol 72:1491–1497.[CrossRef][Medline] [Order article via Infotrieve]
  • Davenport ES, Williams CE, Sterne JA, Murad S, Sivapathasundram V, Curtis MA (2002). Maternal periodontal disease and preterm low birthweight: case-control study. J Dent Res 81:313–318.
  • Dörtbudak O, Eberhardt R, Ulm M, Persson GR (2005). Periodontitis, a marker of risk in pregnancy for preterm birth. J Clin Periodontol 32:45–52.[CrossRef][Medline] [Order article via Infotrieve]
  • Ewing JA (1984). Detecting alcoholism. The CAGE questionnaire. J Am Med Assoc 12:1905–1907.
  • Flores-de-Jacoby L, Bruchmann S, Mengel R, Zafiropoulos GGK (1991). Periodontal conditions in Rio de Janeiro city (Brazil) using the CPITN. Community Dent Oral Epidemiol 19:127–128.[Medline] [Order article via Infotrieve]
  • Hathaway SR, McKinley JC (1943). The Minnesota Multiphasic Personality Inventory. Minneapolis: University of Minnesota Press.
  • Jarjoura K, Devine PC, Perez-Delboy A, Herrera-Abreu M, D’Alton M, Papapanou PN (2005). Markers of periodontal infection and preterm birth. Am J Obstet Gynecol 192:513–519.[CrossRef][Medline] [Order article via Infotrieve]
  • Jeffcoat MK, Geurs NC, Reddy MS, Cliver SP, Goldenberg RL, Hauth JC (2001). Periodontal infection and preterm birth: results of a prospective study. J Am Dent Assoc 132:875–880.[Abstract/Free Full Text]
  • Jeffcoat MK, Hauth JC, Geurs NC, Reddy MS, Cliver SP, Hodgkins PM, et al. (2003). Periodontal disease and preterm birth: results of a pilot intervention study. J Periodontol 74:1214–1218.[CrossRef][Medline] [Order article via Infotrieve]
  • Leal MdoC, da Gama SG, Ratto KMN, Cunha CB (2004). Use of the modified Kotelchuck index in the evaluation of prenatal care and its relationship to maternal characteristics and birth weight in Rio de Janeiro, Brazil. Cad Saude Publica 20(Suppl 1):63S–72S.
  • López NJ, Smith PC, Gutierrez J (2002). Higher risk of preterm birth and low birth weight in women with periodontal disease. J Dent Res 81:58–63.
  • Lunardelli AN, Peres MA (2005). Is there an association between periodontal disease, prematurity and low birth weight? A population-based study. J Clin Periodontol 32:938–946.[Medline] [Order article via Infotrieve]
  • Madianos PN, Bobetsis GA, Kinane DF (2002). Is periodontitis associated with an increased risk of coronary heart disease and preterm and/or low birth weight births? J Clin Periodontol 29(Suppl 3):22–36.
  • Marin C, Segura-Egea JJ, Martinez-Sahuquillo A, Bullon P (2005). Correlation between infant birth weight and mother’s periodontal status. J Clin Periodontol 32:299–304.[CrossRef][Medline] [Order article via Infotrieve]
  • Michalowicz BS, Hodges JS, DiAngelis AJ, Lupo VR, Novak MJ, Ferguson JE, et al. (2006). Treatment of periodontal disease and the risk of preterm birth. N Engl J Med 355:1885–1894.[Abstract/Free Full Text]
  • Mitchell-Lewis D, Engebretson SP, Chen J, Lamster IB, Papapanou PN (2001). Periodontal infections and pre-term birth: early findings from a cohort of young minority women in New York. Eur J Oral Sci 109:34–39.[CrossRef][Medline] [Order article via Infotrieve]
  • Moliterno LF, Monteiro B, Figueredo CM, Fischer RG (2005). Association between periodontitis and low birth weight: a case-control study. J Clin Periodontol 32:886–890.[Medline] [Order article via Infotrieve]
  • Moore S, Ide M, Coward PY, Randhawa M, Borkowska E, Baylis R, et al. (2004). A prospective study to investigate the relationship between periodontal disease and adverse pregnancy outcome. Br Dent J 197:251–258.[CrossRef][Medline] [Order article via Infotrieve]
  • Offenbacher S, Katz V, Fertik G, Collins J, Boyd D, Maynor G, et al. (1996). Periodontal infection as a possible risk factor for preterm low birth weight. J Periodontol 67(10 Suppl):1103–1113.[Medline] [Order article via Infotrieve]
  • Offenbacher S, Lieff S, Boggess KA, Murtha AP, Madianos PN, Champagne CM, et al. (2001). Maternal periodontitis and prematurity. Part I: Obstetric outcome of prematurity and growth restriction. Ann Periodontol 6:164–174.[CrossRef][Medline] [Order article via Infotrieve]
  • Radnai M, Gorzó I, Nagy E, Urbán E, Novák T, Pál A (2004). A possible association between preterm birth and early periodontitis. A pilot study. J Clin Periodontol 31:736–741.[CrossRef][Medline] [Order article via Infotrieve]
  • Rajapakse PS, Nagarathne M, Chandrasekra KB, Dasanayake AP (2005). Periodontal disease and prematurity among non-smoking Sri Lankan women. J Dent Res 84:274–277.
  • Sokol RJ, Martier SS, Ager JW (1989). The T-ACE questions: practical prenatal detection of risk-drinking. Am J Obstet Gynecol 160:863–871.[Medline] [Order article via Infotrieve]
  • Spielberger CD, Gorsuch RL, Lushene RE (1970). Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologist Press.
  • Vasconcelos MTL, Anjos LA (2003). A simplified method for assessing physical activity level values for a country or study population. Eur J Clin Nutr 57:1025–1033.[Medline] [Order article via Infotrieve]
  • Vettore MV, Lamarca GA, Leão AT, Thomaz FB, Sheiham A, Leal MC (2006). Periodontal infection and adverse pregnancy outcomes: a systematic review of epidemiological studies. Cad Saude Publica 22:2041–2053.[Medline] [Order article via Infotrieve]

Journal of Dental Research, Vol. 87, No. 1, 73-78 (2008)
DOI: 10.1177/154405910808700113
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