Australian and New Zealand Journal of Obstetrics and Gynaecology 2004; 44: 568–573
Original Article
Blackwell Publishing, Ltd.
Periodontal diseases and pre-eclampsia
Periodontal disease as a risk factor for pre-eclampsia: A case control study Varol CANAKCI,1 Cenk Fatih CANAKCI,1 Hümeyra CANAKCI,2 Ebru CANAKCI,3 Yasin CICEK,1 Metin INGEC,2 Mehmet OZGOZ,1 Turgut DEMIR,1 Alparslan DILSIZ1 and Hatice YAGIZ1 1
Department of Periodontology, School of Dentistry, 2Department of Obstetrics and Gynecology, School of Medicine, and 3Department of Anaesthesiology and Reanimation, Ataturk University, Erzurum, Turkey
Abstract Objective: To investigate the association between periodontal disease and pre-eclampsia, while controlling known risk factors for pre-eclampsia. Methods: A matched case-control study was carried out on 41 pre-eclamptic women and 41 normotensive, healthy, pregnant, control women. The pre-eclamptic women and controls were individually matched for age, gravidity, parity, smoking and prenatal care. The number of teeth and the number of restorations and decay on all tooth surfaces, and clinical periodontal parameters, excluding third molars were determined within 48 h before delivery. The relation of independent variables to pre-eclampsia was assessed using conditional multiple logistic regression analysis on subject-based data. Results: There were no statistically significant differences in mean percentages of sites with plaque between groups. The mean probing depth (PD) and mean clinical attachment level (CAL) for pre-eclamptic patients were significantly greater compared to those of normotensive patients (P < 0.01). The percentage of sites exhibiting bleeding on probing (BOP) (P < 0.05), the number of sites with PD ≥ 4 mm and with CAL ≥ 3 mm was significantly higher among pre-eclamptic patients than those with normotensive patients (P < 0.01). Conditional multiple logistic regression analysis indicated that periodontal disease and triglycerides level were significantly associated with pre-eclampsia. Other independent variables (maternal body weight and serum total cholesterol level) did not appear to be associated with pre-eclampsia. Conditional multiple logistic regression results showed that pre-eclamptic patients were 3.47 (95% CI = 1.07 –11.95) times more likely to have periodontal disease than normotensive patients. Conclusion: The present study shows that maternal periodontal disease during pregnancy is associated with an increased risk for the development of pre-eclampsia. The higher incidence of periodontal disease parameters in preeclamptic group would suggest a possible role for periodontal disease in the development of pre-eclampsia. The nature both of periodontitis and pre-eclampsia is multifactorial, and caution should be exercised when implicating periodontal disease in causation of pre-eclampsia. Key words: periodontal diseases, pre-eclampsia, risk factors.
Introduction Pre-eclampsia is a dangerous disease of human pregnancy, which affects both the mother and her fetus.1 It is a common obstetric syndrome affecting approximately 7 –10% of pregnant women and remains one of the two most common causes of maternal mortality in the developed world.2,3 There are two syndromes in pre-eclampsia. The first is maternal, characterised by endothelial cell activation, hypertension and proteinuria. The second is fetal, manifested primarily by intrauterine growth restriction. The symptoms of this syndrome appear during the second and third trimester of pregnancy.2–4 568
Although this disease is of major obstetric importance throughout the world, it remains enigmatic.1,5 Despite extensive research, neither its cause nor possible mechanism has been clearly defined.1,5–7 In other words, pre-eclampsia should probably be regarded as a syndrome of heterogeneous origin.6 Different factors have been postulated to be contributory, genetic, immune, obesity, hormone and race.1,7–10
Correspondence: Dr Varol Canakci, Atatürk Üniversitesi, Dis HekimliGi Fakültesi, Periodontoloji Ana Bilim Dalı, 25240, Erzurum, Turkey. Email:
[email protected] Received 14 April 2004; accepted 27 July 2004.
Periodontal diseases and pre-eclampsia
The known risk factors for pre-eclampsia include primiparity (first birth), nulligravidity (no pevious pregnancy), obesity, renal disease, uterine malformation, fetal hydrops, elevated serum lipid ratio, non-smoking, no prenatal care and diabetes.6,11,12 However, during recent years, the concept of focal infection has been examined with interest.3,5 It has been reported that infection can be important in the pathogenesis of pre-eclampsia, both in term of its initiation and /or its potentiation.3,5 New attention is focused on infectious agents as possible causes of a disease that were earlier considered to be caused by genetic disposition or lifestyle factors.5 The mechanisms described in the development of atherosclerosis resemble the pathophysiological mechanisms described in preeclampsia, and have been associated with infectious agents.3,5 It has been shown that pre-eclampsia is associated with preterm low birth weight.13 Researchers have reported that early onset pre-eclampsia is associated with placental vascular lesions or reduced uteroplacental blood supply leading to reduced birth weight.8,14,15 Periodontal diseases are traditionally regarded as chronic inflammatory oral infections in which bacteria and their byproducts are the principal aetiologic agents.16–18 Recent studies indicate that this oral disease can have profound effects on systemic health.17 Studies conducted on different populations have suggested that atherosclerosis could be linked with chronic oral infections.19,20 In a preliminary study, gram negative periodontal pathogens were seen on atheromatous plaques.21 Likewise, periodontal disease appears to be an independent risk factor for preterm/term low birth weight.22–25 In light of the studies mentioned earlier, it is hypothesised that a relationship exists between periodontal diseases and pre-eclampsia. Therefore, the purpose of the present study was to investigate the possible association between periodontal disease and pre-eclampsia, while controlling known risk factors for pre-eclampsia (parity, gravidity, non-smoking, and prenatal care).
All 68 eligible cases that were approached agreed to participate in the study. Twenty-seven pre-eclamptic women were excluded from these analyses because of matching and exclusion criteria. Controls were normotensive pregnant women and were selected from pregnant women who delivered within 48 h before or after the delivery of the case pregnant women. Controls were selected from the same hospital and the same population as the cases. Pre-eclamptic women and controls were individually matched for age (within 1 year), parity, gravidity, smoking and prenatal care. Thus, 41 preeclamptic women (group 1) and 41 normotensive healthy control women (group 2) were included in this study. Age, marital status, prenatal care and medical histories pertaining to the exclusion criteria were obtained according to hospital records. Education level of each mother, household income and information about smoking (at least three cigarettes per day) and alcohol use were obtained through a personal interview conducted by a trained physician at the first prenatal visit. Both groups of women had similar ethnic origin (Turkish). None of these patients had a history of endocrine disorders (diabetes mellitus, phaeochromocytoma, thyrotoxicosis, etc.), polycystic ovary syndrome, uterine malformation, renal disease, collagen vascular disease (lupus, scleroderma), coarctation of the aorta, chronic hypertension, heart murmur or valvular heart disease They did not receive antibiotic prophylaxis for dental treatment and any medication that might have influenced sex steroid metabolism. They had not received periodontal therapy up to 6 months prior to the study. This study was approved by our ethics committee and a written informed consent was obtained from each participant.
Materials and methods
Dental examination
Patient selection
The number of teeth and the number of restorations and decay on all tooth surfaces, and clinical periodontal parameters, excluding third molars were determined within 48 h prior to delivery. Third molars are rarely absent or do not often erupt in the mouths of young individuals (particularly18 –25 year olds). All examinations were performed by two trained and calibrated examiners (periodontists) who were not aware of the information the female patients had given in the interview. Each tooth, excluding third molars, was measured and examined for periodontal pocket depth (PD) in mm and clinical attachment level (CAL) (in mm at six sites per tooth – mesiobuccal, direct buccal, distobuccal, mesiolingual, direct lingual, and distolingual) with a Williams’ probes with Michigan markings (Hu-Friedy). The PD was determined by measuring the distance from the free gingival margin to the base of the pocket. The CAL was measured as the distance between enamel–cementum junction and the base of the pocket. Dental plaque was scored as being present or absent at the four
A matched case-control study with a selection ratio of 1 was performed using 41 women with pre-eclampsia. Forty-one controls (without the complication of pre-eclampsia) were recruited from among pregnant women at the departments of obstetrics and gynecology of the medical faculty in Erzurum in 2002. Women were diagnosed with pre-eclampsia if they had (i) blood pressures of at least 140 /90 mmHg on two or more occasions at least 4 h apart after 20 weeks’ gestation and (ii) proteinuria, which was considered present when one 24-h urine collection showed a total protein excretion of at least 300 mg or when there was a urine dipstick value of at least 1 + (30 mg /dL) on two separate occasions at least 6 h apart if a 24-h urine specimen was unavailable (American College of Obstetricians and Gynecologists, 1966).26 The pre-eclamptic patients were healthy before the onset of pre-eclampsia.
Laboratory analysis Blood samples (approximately 30 cc of blood drawn from the antecubital vein of each patient) were taken on admission. Serum total cholesterol and triglycerides were determined by autoanalyser in the clinical laboratory.
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points (mesial, buccal, lingual and distal) on each tooth. Bleeding on probing (BOP) was assessed on the six sites at which PD was determined and deemed positive if it occurred within 15 s after probing. Bleeding on probing was expressed as the percentage of sites showing bleeding. Examiners were thoroughly trained and calibrated in the recording of the probing department and clinical attachment level measurements. Intra-examiner variability in using the dental examination criteria was tested by performing duplicate examinations on 12 randomly selected mothers on consecutive days. Corresponding percentages of agreement were 89% for probing depth and bleeding, and 86% for clinical attachment level. Neither the interviewer or the examiners were aware of the case-control status of the subject at the time of the interview or examination. The presence of four or more teeth with one or more sites with PD ≥ 4 mm that bled on probing, and with a clinical attachment loss ≥ 3 mm at the same site, was diagnosed as periodontal disease.
Data analysis Data were analysed using a SAS Statistical Package for Windows version 6.1 (SAS Institute Inc., Cary, NC). Chi-square analyses were used to test the group differences in categorical variables. Student t-test and non-parametric tests were used for test the group differences in continuous variables. Multivariate analyses were performed using conditional logistic regression while taking matching into consideration. The odds ratios (OR) and 95% confidence intervals (95% CI)
were obtained to indicate the association between a potential risk factors and pre-eclampsia using the stepwise procedure. For categorical variables, the regression coefficients obtained from the models estimate the natural logarithm of the ratio of odds of having pre-eclampsia in one group compared to the other. For continuous variables such as periodontal disease, the regression coefficient estimates the increase in log odds for pre-eclampsia per unit increase in that variable. For all statistical tests, two-sided type I error probability = 0.05 was considered as the level of significance.
Results The characteristics of the two groups of pregnant patients are shown in Table 1. There were no significant differences in mean age, gravidity, parity, smoking, prenatal care, marital status, alcohol use, education level and household income between the two-group patients (P > 0.05). None of the pregnant patients drank alcohol, and all were married. Pregnancy-related characteristics of the pre-eclamptic and normotensive patients are shown in Table 2. There were significant differences in the duration of gestation, birth weight, systolic and diastolic blood pressure, body weight in the third trimester, prenatal care, serum cholesterol and triglycerides level between the pre-eclamptic and normotensive patients. Table 3 displays the clinical dental and periodontal variables in two group patients. The number of present teeth, decayed and restorations in two group patients were similar (P > 0.05). There were no statistically significant differences in
Variable
Pre-eclamptic patients
Normotensive controls
P value
Age (year) Married (%) Gravidity (mean ± SD) Parity (mean ± SD) Education (years) Household income ($) Smoking (%) (yes) Alcohol (%) (yes) Prenatal care (%) (yes)
25.9 ± 5.9 100% 1.61 ± 0.9 0.53 ± 0.7 7.42 ± 5.1 327.4 ± 117.2 19.5% 0 34.1%
25.8 ± 5.8 100% 1.65 ± 0.9 0.55 ± 0.7 8.2 ± 5.6 338.5 ± 105.8 19.5% 0 34.1%
0.955 NS 0.726 0.768 0.830 NS NS NS NS
Table 1 Demographic characteristics (mean ± standard deviation) of pre-eclamptic and normotensive control patients (n = 41 each)
NS, not significant.
Variables
Pre-eclamptic patients
Normotensive controls
P value
Gestation (week) Body weight in the third trimester (kg) Systolic blood pressure (mm / Hg) Diastolic blood pressure (mm / Hg) Birthweight (g) Serum cholesterol level (mg / dL) Triglycerides level (mg / dL)
34.7 ± 0.8 79 ± 12.4 179.4 ± 3.1 119.3 ± 2.6 2098 ± 92.6 239.2 ± 42.9 198.4 ± 55.8
39.1 ± 0.4 69.4 ± 11.2 108.9 ± 1.6 62.8 ± 1.8 3416 ± 62.9 179.9 ± 36.3 151.4 ± 47.4
0.001** 0.041* 0.001** 0.001** 0.001** 0.032* 0.029*
Table 2 Pregnancy-related characteristics (mean ± standard deviation) of pre-eclamptic and normotensive control patients (n = 41 each)
*P < 0.05; **P < 0.001, significant differences between the two groups.
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Periodontal diseases and pre-eclampsia Table 3 Clinical dental and periodontal variables in pre-eclamptic and normotensive control patients (n = 41 each)
Variable
Pre-eclamptic patients
Dental parameters Number of teeth (mean ± SD) Decayed (mean ± SD) Restored (mean ± SD) Periodontal parameters at delivery Mean PD (mm) Mean CAL (mm) % of sites PD ≥ 4 mm CAL ≥ 3 mm % sites with Plaque % sites exhibiting BOP Periodontal Disease (yes) (n and %)
Normotensive controls
P value
23.9 ± 6.9 4.1 ± 4.4 7.9 ± 6.3
24.7 ± 7.1 3.8 ± 3.9 7.4 ± 5.6
0.723 0.604 0.745
2.99 ± 0.38 3.25 ± 0.49
2.34 ± 0.31 2.51 ± 0.45
0.003** 0.005**
21.2 ± 9.7 27.3 ± 10.9 67.7 ± 24.7 40.6 ± 13.9 24 (46.3%)
12.1 ± 9.2 14.7 ± 9.9 67.9 ± 24.8 24.7 ± 11.8 11 (21.9%)
0.010** 0.003** 0.843 0.021* 0.019**
BOP, bleeding on probing; CAL, clinical attachment level; PD, probing depth. NS, not significant; *P < 0.05, **P < 0.01, significant differences between the two groups.
Table 4 Factors associated with pre-eclampsia: Conditional multiple logistic regression model Risk factor Periodontal disease Maternal body weight ≥ 75 kg Serum triglyceride ≥ 100 mg / dL Serum cholesterol ≥ 200 mg / dL
Coefficient
Standard error
Odds ratio Z
95% CI
P value P > |z|
1.245 0.595 1.174 0.324
0.631 0.754 0.536 0.744
3.47 1.73 3.07 1.38
1.07– 11.95 0.42– 7.95 1.13 –9.25 0.32– 5.94
0.037* 0.430 0.029* 0.598
CI, confidence intervals; *P < 0.05; **P < 0.01, significant differences.
mean percentages of sites with plaque between groups. The mean PD and mean CAL for pre-eclamptic patients were significantly greater as compared with those of normotensive patients (P < 0.01). The mean PD was higher in pre-eclamptic patients (2.99 mm) than in normotensive patients (2.34). Similarly, the values for the mean CAL were 3.25 mm and 2.51 mm, respectively. The percentage of sites exhibiting BOP, the number of sites with PD ≥ 4 mm and with CAL ≥ 3 mm were significantly higher among pre-eclamptic patients than normotensive patients. The percentage of sites exhibiting BOP were found in 40.6% of the pre-eclamptic group and 24.7% of the normotensive group (P < 0.05). Sites with PD ≥ 4 mm were 21.2% in the pre-eclamptic group and 12.1% in the normotensive group (P < 0.01). Similarly, sites with CAL ≥ 3 mm were found in 27.3% in the pre-eclamptic group and 14.7% in the normotensive group (P < 0.01). Periodontal Disease (the presence of four or more teeth with one or more sites with PD ≥ 4 mm that bled on probing, and with a clinical attachment loss ≥ 3 mm at the same site) was found in 46.3% of the pre-eclamptic group and 21.9% of the normotensive group (P < 0.01). The results of the final conditional multiple logistic regression model are shown in Table 4. Variables found to be associated with pre-eclampsia (periodontal disease, serum cholesterol level, serum triglycerides level, and maternal body weight ≥ 75 kg) were then included in the multiple logistic regression model. Conditional multiple logistic regression
analysis indicated that periodontal disease, and serum triglycerides level were significantly associated with pre-eclampsia. Other independent variables (maternal body weight ≥ 75, serum total cholesterol level) did not appear to be associated with pre-eclampsia. Conditional multiple logistic regression results showed that pre-eclamptic patients were 3.47 (95% CI = 1.07–11.95) times more likely to have periodontal disease than normotensive patients. Serum triglyceride level was 3.07 (95% CI = 1.13–9.25) times as high in pre-eclamptic patients than that normotensive patients.
Discussion The hypothesis that periodontal disease is associated with pre-eclampsia was tested by using a matched case-control study. Periodontal disease and elevated serum lipid ratio emerged as independent risk factors for pre-eclampsia in the present study. Some of the known risk factors for preeclampsia such as maternal body weight and serum total cholesterol level were not found to be significantly associated with pre-eclampsia in this group of patients. In the present study, pre-eclamptic cases were matched with normotensive case controls in order to minimise confounding of the primary association with age, gravidity, parity, smoking and prenatal care. The confounding effect of the
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other known risk factors for pre-eclampsia was handled at the analytic stage through appropriate statistical models. In light of the above-mentioned points, we observed an association with serum triglyceride level, one of the known associations for pre-eclampsia. Validity of our results can be examined in light of change, potential bias, and confounding. Since there were no estimates on the association between periodontal disease and preeclampsia in the literature at the time of the study, our sample size calculation was not based on this primary hypothesis. However, 41 case-control pairs seemed adequate for testing the known associations. Patients in the pre-eclamptic group had worse periodontal health than those in the normotensive at delivery group. Periodontal disease was found in 46.3% of pre-eclamptic patients and 21.9% of normotensive patients. Gingival bleeding was more common among pre-eclamptic patients than normotensive patients. However, plaque was assessed dichotomously since it has been shown that the amount of supragingival plaque present at an individual site was not related to the severity of periodontal destruction.27,28 There was no significant difference in the percentages of sites with plaque deposits between the two groups. While it could be possible that pregnant patients with complication tend to have more plaque deposits because of limited dexterity, this concept was not validated in our study. From the similar amount of plaque in the two groups, it could be inferred that the amount of destruction seen in the pre-eclamptic group could be attributed to the content (quality) of the plaque or the other factors. The present study shows that maternal periodontal disease during pregnancy is associated with an increased risk for the development of pre-eclampsia. It has been suggested that the mechanisms described in the development of atherosclerosis resemble the pathophysiological mechanisms described in pre-eclampsia, and are associated with infectious agents.3,5 There is evidence that chronic infection can be an important cofactor in initiating atherogenesis, and these epidemiological data support the premise that chronic infection could link pre-eclampsia with later atherosclerosis, especially given the increased susceptibility to chronic infection because of reduced cell-mediated immunity in pregnancy.3,29 However, studies conducted on different populations have suggested that atherosclerosis could be linked with chronic oral infections.19,20 Recently, it has been demonstrated that several candidate periodontal pathogens, including Porphyromanas gingivalis, can be detected in atheromatous plaque.21,30 It is possible that these pathogens can similarly promote and modify pre-eclampsia sharing the mechanisms described in the development of atherosclerosis. It is suggested that periodontal disease, which causes chronic inflammation, can in turn be linked with pre-eclampsia. The present study indicated that serum triglyceride levels were approximately three times as high in pre-eclamptic patients as those found in normotensive patients. A number of studies have also documented a relationship between infection and hyperlipidemia.18,31–34 Cutler et al.32 indicated that the presence of a significant relationship between periodontitis, 572
hyperlipidaemia and serum antibodies against Porphyromanas gingivalis LPS. A chronic hyperlipidaemic state can impair the host resistance to bacterial infection, while promoting the destruction of periodontal tissues. It has been also reported that pre-eclamptic pregnancy is associated with a marked hyperlipidaemia.3,34,35 In short, both periodontitis and preeclampsia are associated with elevated triglycerides level. Therefore, the results of the present study could suggest evidence for a causal link between periodontal disease and pre-eclampsia. There was significant difference in maternal body weight in the third trimester between the pre-eclamptic and normotensive, but the results of multiple logistic regression did not confirm the statistically significant associations observed in test. Maternal body weight and prenatal care, known as risk factors for pre-eclampsia in other studies,9,36 were not observed as risk factors in our study. Preterm low birth and preterm delivery were not included in the statistical model of the present study. Preterm delivery is often seen in pre-eclamptic pregnancies and, in most cases, is a result of induction of delivery because of the risk to the mother and the baby if the pregnancy continues. In other words, pre-eclampsia can be a cause of iatrogenic preterm birth and small-for-gestational-age infants.8,13–15 Investigators have demonstrated significant associations between periodontitis and preterm low birth weight.22,25 The preeclamptic patients in the present study had a significantly increased incidence of preterm delivery and periodontal disease. One possibility is that worsening of the maternal periodontal status during pregnancy could reflect an increase in placental infectious /inflammatory stimuli, which in turn can intensify the already elevated inflammatory status of preeclamptic patients, leading to an increased risk of preterm delivery. From the present case-control study, we can conclude that the higher periodontal disease parameters in the preeclamptic group would suggest a possible role for periodontal disease in the development of pre-eclampsia. The nature of both periodontitis and pre-eclampsia is multifactorial, and caution should be exercised when implicating periodontal disease in causation of pre-eclampsia. If the observed association between pre-eclampsia and periodontal disease parameters is indeed causal in nature, there are important implications for the clinician in that reductions in periodontal infections in the pregnancy population would be expected to result in a reduced incidence and /or complications from preeclampsia. Additional studies, using similar methodology in other populations, are needed to corroborate these results.
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