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Periodontal Disease and Prematurity among Non-smoking Sri Lankan Women

¹ University of Peradeniya Faculty of Dental Sciences and
² Matale Base Hospital, Sri Lanka; and
³ Department of Epidemiology and Health Promotion, New York University College of Dentistry, 345 East 24th Street, New York, NY 10010, USA;

^* corresponding author, Ad75{at}NYU.edu

	ABSTRACT

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The hypothesis that periodontal disease is associated with pre-term low birthweight was tested in a prospective follow-up study of rural prima-gravida women (N = 227) who were free of tobacco, alcohol, and drug use. Women with 3rd trimester mean probing pocket depths, plaque, and bleeding scores that were greater than the median value in the cohort were defined as ‘exposed’. There were 17 (7.5%) preterm low birthweight singleton deliveries in the cohort (among ‘exposed’ = 12%; among ‘unexposed’ = 5.6%; Odds Ratio = 2.3; 95% CI = 0.9–6.3). After adjustment for the independent variables, the OR for preterm low birthweight in relation to ‘exposure’ was 1.9 (95% CI = 0.7–5.4). Our results are only suggestive of an association between periodontal disease and preterm low birthweight, perhaps indicating that previously reported associations may have been subjected to residual confounding due to tobacco, alcohol, and drug use.

KEY WORDS: prematurity • low birthweight • periodontal disease • non-smokers • Sri Lanka

	INTRODUCTION

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Maternal periodontal disease is emerging as an independent risk factor for preterm delivery and low birthweight. Periodontal pathogens have been detected in amniotic fluid of preterm delivery cases with chorioamnionitis (Dixon et al., 1994) or in the homogenized cord (Wright et al., 1994). Elevated periodontal pathogen levels are seen in the oral cavities of women who deliver preterm low birthweight infants (Offenbacher et al., 1998, 2001). Clinical periodontal disease has been associated with preterm low birthweight in some studies (Offenbacher et al., 1996, 2001; Dasanayake, 1998; Jeffcoat et al., 2001; Lopez et al., 2002a), while other studies have failed to observe such an association (Offenbacher et al., 1998; Mitchell-Lewis et al., 2001; Davenport et al., 2002). Periodontal pathogen-specific serum IgG levels are either positively (Dasanayake et al., 2001) or negatively associated with preterm low birthweight (Madianos et al., 2001), and periodontal treatment during pregnancy has resulted in a significant reduction of preterm low birthweight in one study (Lopez et al., 2002b), while the reduction was not significant in another (Jeffcoat et al., 2003).

The above discrepancies of results among studies may be due to study limitations such as small sample size, assessment of periodontal status after delivery, insufficient control for key confounding variables, and the inadequacy of the clinical assessment of periodontal disease as an indicator of the underlying biology associated with periodontal disease. An additional explanation for the negative studies, particularly the studies from Europe, is the possibility that the association is modified by some population-specific characteristics such as the differential rates of disease and potential exposures and other risk factors. Further studies conducted in distinct populations that evaluate various aspects of periodontal disease in relation to prematurity are needed before we can better understand the potential role of periodontal disease in pregnancy outcomes. If these studies are conducted in populations that are free of major risk factors for poor pregnancy outcomes, such as smoking, alcohol, and drug abuse, relatively unconfounded estimates for the proposed association can be obtained.

In this study, we have evaluated the association between clinical periodontal disease and prematurity using a group of 18- to 34-year-old rural Sri Lankan primiparous women who are free of smoking, alcohol, and drug use. Our hypothesis was that there is no association between clinical periodontal disease and preterm low birthweight among rural Sri Lankan women who do not smoke or chew tobacco, drink alcohol, or use drugs.

	MATERIALS & METHODS

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A prospective follow-up study was conducted in Matale, Sri Lanka. Matale is located in the central hills of Sri Lanka and has a population of 442,427 (2003 census), most of whom live in rural areas (384,209). The median annual household income of the local population is below $400. Two hundred and twenty-seven primiparous women who were free of maternal hypertension, diabetes, smoking and betel chewing, and alcohol and drug abuse were recruited during the late third trimester of pregnancy, when they presented themselves to the Base Hospital in Matale for pre-natal care. Additional eligibility criteria were that they be between 18 and 34 years of age and had no history of past periodontal treatment during pregnancy. Following written informed consent, according to the institutional review board of Peradeniya University guidelines, the periodontal disease level of each eligible subject was measured with the use of a pressure-controlled periodontal probe (Brodontic^®, Prima, Byfleet, England) that was set at 20 g. Probing pocket depths in relation to 4 sites per tooth (mesial, distal, facial, and lingual) were measured in all erupted teeth except for the third molars. Gingival bleeding on gentle probing was recorded according to the Silness and Löe index (Silness and Löe, 1964), and plaque levels were recorded according to the O’Leary plaque index (O’Leary, 1967) in relation to the same surfaces. Mean pocket depth (PD), plaque scores (PL), and bleeding scores (BL) were calculated for each subject. All examinations were performed at the dental clinic of the hospital by one clinician (KBC), who was calibrated against an experienced investigator (PSR) with 95% inter-examiner agreement.

The ‘exposure’ was defined as having mean PD, PL, and BL scores that are greater than the median value in the total cohort, either individually or in combination. Preterm low birthweight was defined as live infants with birthweight less than 2500 g, who were delivered before 37 wks of gestation. Gestational age was based on ultrasound examinations in all subjects. Birthweight was obtained from hospital records. The same scale was used in obtaining the birthweight of all subjects.

Demographic data, past dental history, and the educational and occupational status of each mother and her spouse were obtained by a questionnaire administered by a trained interviewer. Occupational status categorization was based on the Registrar General’s classification. Obstetric history, parity, last menstrual period, expected date of delivery, risk conditions, past medical history, care given at the pre-natal clinic, height and weight of the gravida, type and date of delivery, and birthweight of the newborn were obtained from hospital records. Weight and height of the gravida were based on the last pre-natal visit.

Based on 20% preterm low birthweight among the subjects with no periodontal disease, and an Odds Ratio of 3 for the association between clinical periodontal disease and preterm low birthweight (Dasanayake, 1998), for a prospective study with 5% Type I error and 95% power, 46 subjects with periodontal disease (exposed group) were required. Assuming 10% loss to follow-up, 51 subjects were needed within the exposed group. We needed to screen 205 subjects to get the required 51 subjects with periodontal disease, based on 25% prevalence of moderate to severe periodontal disease among the target population (based on national surveys, 16–43% of women have either shallow or deep pockets) (Ministry of Health, 1995). We studied 227 subjects, resulting in a cohort of 66 subjects with the ‘exposure’ and 161 without the ‘exposure.

Data were analyzed by logistic regression analysis. Preterm low birthweight (yes or no) was used as the dependent variable, with adjustment for the independent variables and interaction terms. Two-sided type I error probability 0.05 was considered as the level of significance.

	RESULTS

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There were 66 women in the ‘exposed’ category (defined as having all 3 individual PL, BL, and PD mean values that are higher than the median values in the total cohort) and 161 women who were not exposed (Table 1). Women in the two groups were in their mid-twenties, were about 153 cm in height, and had a BMI of about 20 at the last pre-natal care visit. Women in the ‘exposed’ group sought pre-natal care significantly later and had significantly less weight at the last pre-natal care visit. When birthweight and gestational age were treated as continuous variables, there were no statistically significant differences between the two groups.

The distribution of preterm low birthweight by individual periodontal disease measures (i.e., PL, BL, and PD scores), as well as the combined measures to denote the ‘exposure’ status, are indicated in Table 2. When each periodontal measure (i.e., mean value for the subject) was dichotomized with the median value in the total cohort, the proportion of preterm low birthweight in the high-PL-score group was 10%, compared with 5% in the low-PL group. The proportion of preterm low birthweight in the group with high BL values was 10.8%, compared with 4.3% in the low-BL group. Similarly, the high-PD group had 10.1% preterm low birthweight, compared with 5.1% in the low-PD group. All of the 95% confidence intervals for the odds ratios for the above associations included the null value of 1 (Table 2). The proportion of preterm low birthweight among ‘exposed’ (i.e., all 3 mean PL, BL, and PD scores are above the median value of the cohort) was 12%, and among ‘unexposed’, 5.6% (OR = 2.3; 95% CI = 0.9–6.3). After adjustment for the significant variables between the two groups that emerged from the univariate analysis (Table 1), the adjusted OR for the association between ‘exposure’ and preterm low birthweight was 1.9 (95% CI = 0.7–5.4).

	DISCUSSION

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One possible mechanism for the association between periodontal disease and prematurity is that these and other micro-organisms, their endotoxins, and resulting host inflammatory mediators can enter the uterine cavity from remote sites, such as the oral cavity, either directly or from the blood-borne route and give rise to another cascade of inflammatory mediators within decidua and membranes. These events can result in either prostaglandin production or direct uterine contractions that can lead to cervical dilation. The dilated cervix can then allow further entry of bacteria, their products, and cytokines to the uterine cavity, until preterm delivery and/or premature rupture of the membranes occurs (Gibbs, 2001).

Based on the above hypothesis, we (Dasanayake, 1998; Dasanayake et al., 2001, 2003) and others (Jeffcoat et al., 2001; Lopez et al., 2002a, b; Offenbacher et al., 1996, 1998, 2001) have demonstrated significant associations among clinical periodontal disease, bacteriological and immunological parameters related to periodontal disease, and preterm low birthweight, while other investigators (Mitchell-Lewis et al., 2001; Davenport et al., 2002) have failed to show such an association.

In this investigation, we studied a group of non-smoking, non-drinking, and non-drug-using women who were pregnant for the first time. The overall preterm low birthweight rate in the study cohort (7.5%) was lower than expected. Among the possible explanations for this finding are: relatively early onset of pre-natal care in this group (12–14 wks), universal access to free health care, and a reasonable nutritional status of the subjects (BMI = 20).

We observed a higher proportion of preterm low birthweight among subjects with higher pocket depths, plaque, and bleeding scores. Similarly, when the 3 periodontal disease measures were combined to define the ‘exposure’ status, the ‘exposed’ group had a marginally significant increase of risk for preterm low birthweight.

Our findings are important for several reasons. First, these women were free of alcohol, smoking, and drug abuse, 3 major risk factors for prematurity in the Western world. Second, they were all first-time pregnancies, hence were free of previous pregnancy-related risk factors. Third, all were from a similar ethnic and socio-economic background, were of similar age and height, and utilized the same hospital for care. The differential educational background and onset of pre-natal care we observed between ‘exposed’ and ‘unexposed’ women were controlled in the analysis.

One explanation for the smaller, statistically non-significant association we observed, compared with larger, significant associations observed by others, may be residual confounding by smoking, alcohol, and drug use in previous studies. Once we controlled for those factors by study design, it is not surprising that the OR is biased toward the null value. Since we had sufficient power to detect an Odds Ratio of 3, the smaller sample size of our study would be an explanation for not rejecting the null hypothesis only if the actual association is less than an OR of 3.

Finally, there exists the possibility that the alleged association between periodontal disease and prematurity is population-specific. This notion is supported in part by the failure of the European studies conducted among Asian immigrants (Davenport et al., 2002) to find such an association. However, there are no biological explanations as to why the hypothesized association might be population-specific. Among the potential contenders for the population-specific nature of the association, although speculative, might be the racial and ethnic differences, higher or lower rates of preterm low birthweight and periodontal disease in different populations, and the differential distribution of related risk factors among populations.

One threat to the validity of our results is the self-reported nature of the data on chewing or smoking of tobacco, alcohol, and drug use. However, in this traditional society, women, especially rural women such as the study subjects, do not indulge in these habits in general, and during pregnancy in particular, since these practices are cultural taboos. Furthermore, the economically disadvantaged group we studied cannot indulge in these practices even if they want to, due to lack of resources. Occasional betel-chewers (there were three subjects in the study who admitted to chewing betel) refrain from this practice during pregnancy, based on the advice received at the pre-natal visits. One can also argue that birthweight and gestational age are biased estimates, since these were based on hospital records. Since all gestational ages were based on ultrasound examinations, as opposed to the pregnant woman’s estimate of the last menstrual period, and birthweight was measured with the same scale, any misclassification of the above variables is likely to be randomly distributed between ‘exposed’ and ‘unexposed’ subjects. This is an unlikely explanation for our non-significant OR.

Our findings only suggest a possible mild to moderate association between periodontal disease and preterm low birthweight among rural Sri Lankan women. This association is independent of tobacco, alcohol, or drug use, and the strength of the association is lower than what has been reported from other populations. Our findings highlight the need for additional epidemiological studies in different populations with different risk profiles for preterm low birthweight.

	ACKNOWLEDGMENTS

 
This study was funded through grants from the University of Peradeniya, Sri Lanka, and the New York University College of Dentistry.

Received March 26, 2004; Last revision November 16, 2004; Accepted December 12, 2004

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