- Email: [email protected]
Periodontal disease and gestational diabetes mellitus
American Journal of Obstetrics and Gynecology (2006) 195, 1086–9
www.ajog.org
Periodontal disease and gestational diabetes mellitus Xu Xiong, MD, DrPH,a,* Pierre Buekens, MD, PhD,a Sotirios Vastardis, DDS, MS,b Gabriella Pridjian, MDc Department of Epidemiology,a Tulane University; Department of Periodontics,b Louisiana State University; Department of Obstetrics and Gynecology,c Tulane University, New Orleans, LA Received for publication March 1, 2006; revised May 31, 2006; accepted June 9, 2006
KEY WORDS Diabetes Gestational diabetes mellitus Periodontal disease
Objective: We examined the relationship between periodontal disease and different types of diabetes in pregnant and nonpregnant women. Study design: This study was based on the data from the third National Health and Nutrition Examination Survey (NHANES III), including 256 pregnant and 4234 nonpregnant women. Women were classified into those with gestational diabetes mellitus (GDM) in current pregnancy, with GDM in previous pregnancy, and with type 1 or 2 diabetes. Results: In pregnant women, the prevalence of periodontitis was 44.8% in women with GDM and 13.2% in nondiabetic women, with adjusted odds ratio (aOR) of 9.11 (95% confidence interval [CI] 1.11-74.9). In nonpregnant women, the prevalence of periodontitis was 40.3% in women with type 1 or 2 diabetes, 25.0% in women with previous history of GDM, and 13.9% in nondiabetic women, with aOR of 2.76 (1.03-7.35) for women with type 1 or 2 diabetes. Conclusion: We found an association between periodontal disease and GDM. Ó 2006 Mosby, Inc. All rights reserved.
Gestational diabetes mellitus (GDM) is carbohydrate intolerance with onset or first detection during pregnancy.1 Although there is still debate on the need of universal screening of pregnant women for GDM, GDM is associated with significantly increased risks of maternal and infant morbidity, including macrosomia, preeclampsia, preterm birth, shoulder dystocia, birth injury, and need for cesarean section.1,2 Women with GDM are at a significantly higher risk of developing type 2
Presented at the Twenty-Sixth Annual Meeting of the Society for Maternal Fetal Medicine, Miami, FL, January 30-February 4, 2006. * Reprint requests: Dr Xu Xiong, Department of Epidemiology, School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA 70112. E-mail: [email protected] 0002-9378/$ - see front matter Ó 2006 Mosby, Inc. All rights reserved. doi:10.1016/j.ajog.2006.06.035
diabetes later in life.3 A recent randomized controlled clinical trial has suggested that treatment of GDM reduces serious perinatal morbidity and mortality.4 This was the first large clinical trial that provided evidence to support the use of screening and treatment for women with GDM. Periodontal disease is one of the most common chronic disorders of infectious origin known in humans. The reported prevalence in adults varies between 10% and 60%, depending on diagnostic criteria.5,6 Periodontal disease refers to an inflammatory condition of the soft tissues surrounding the teeth (ie, gingivitis) and the destruction of the supporting structures of the teeth, including the periodontal ligament, bone, cementum, and soft tissues (ie, periodontitis).7 There is increasing evidence suggesting that periodontal disease is
Xiong et al associated with an increased risk of systemic diseases such as cardiovascular diseases, diabetes mellitus, and adverse pregnancy outcomes.6,8 The association between periodontal disease and type 1 or 2 diabetes has been well established. Studies have found not only that type 1 or 2 diabetes increases the risk of developing periodontal disease; periodontal disease may also increase the risk for type 1 or 2 diabetes.9 However, based on our recent systematic review,6 no study has examined the relationship between periodontal disease and gestational diabetes mellitus (GDM). The objective of this study was to examine the relationship between periodontal disease and GDM in pregnant women and type 1 or 2 diabetes in nonpregnant women of childbearing age between 15 and 44 years.
Material and methods Population The study population was a sample from the third National Health and Nutrition Examination Survey (NHANES III). NHANES III was a nationally representative cross-sectional survey of the US civilian, noninstitutional population between 1988 and 1994. A detailed description of the plan and operation of NHANES III has been given elsewhere.10 Because our main interest was GDM and its association with periodontal disease, the data included for this analysis were restricted to women who reported to be pregnant during the survey and women who were of childbearing age between 15 and 44 years. In the NHANES III sample, there were a total of 5317 women who were aged between 15 and 44 years. Among them, 290 women were self-reported to be pregnant at the time of survey. After excluding women who did not complete a periodontal examination (419), or did not have information of diabetes status (361), or had both of these conditions (47), the present study sample included 256 pregnant women and 4234 nonpregnant women aged 15 to 44 years.
1087 standard for periodontal disease diagnosis. In most previous studies, definitions that combined PD and CAL over a certain threshold have been used.6 For this study, periodontal disease (ie, periodontitis) was defined as at least 1 site with CAL or PD R4 mm.11 The independent variables of interest were pregnancy and diabetes status. Pregnancy status was determined based on the question of whether women were pregnant at the time of survey. Diagnosis of diabetes was made from the questions of whether women had ever been told by a doctor or other health professional that they had diabetes; whether the diagnosis had been made during pregnancy; and furthermore, whether they had also been told after or outside of pregnancy that they had diabetes. Based on self-reported diabetes status, women were classified into those with type 1 or 2, with GDM in the current pregnancy and with GDM in a previous pregnancy. The main covariates included race/ ethnicity (defined as non-Hispanic black, non-Hispanic white, and Mexican American), age at interview (recoded as !20, 20-35, O35 years old), marital status (married, single, divorced, widowed), years of education (!12 years, R12 years), smoking status (current smoker, former smoker, never smoker), and time elapsed since last dental visit (%6 months, O6 months, R1 year).
Statistical analyses Univariate analysis was performed to compare the difference in prevalence of periodontal disease between the different types of diabetes and nondiabetic groups according to pregnant and nonpregnant status. Odds ratios (OR) and 95% confidence interval (CI) were calculated. Multivariate logistic regression was performed to further examine the association between periodontal disease and the different types of diabetes, adjusting for age, race/ethnicity, smoking, education, and other confounding variables. Because of the complex survey design used in NHANES III, all analyses were conducted by using the software SUDAAN,12 which provided unbiased standard error estimates by taking into consideration the sampling weights provided in the data set.
Study variables Diagnosis and assessment of periodontal disease is based on clinical criteria. The amount of tissue destruction in periodontitis can be measured by the clinical attachment level (CAL, the distance between the cemento-enamel junction and the apical part of the pocket) and probing depth (PD, the distance from the gingival margin to the apical part of the pocket), using a periodontal probe. In NHANES III, oral health examinations were conducted in mobile examination centers by trained and calibrated dental examiners.10 A maximum of 14 teeth and 28 sites were examined for each participant. There is no universally accepted
Results The Table presents prevalence of periodontitis in pregnant and nonpregnant women with and without different types of diabetes. Overall, among 4490 women aged 15 to 44 years, 75.9% of them were white, 16.8% were black, and 7.3% were Mexican and of other origin; 70% were married, and 33.7% smoked (18.5% for pregnant women). Among the study sample, 81 (1.8%) women had GDM in current or previous pregnancies; 70 (1.6%) had type 1 or 2 diabetes. Among 256 pregnant women, 11 had GDM (4.3%).
1088 Table
Xiong et al Periodontal disease and diabetes in pregnant and nonpregnant women, based on NHANES III, 1988-1994
Diabetes Gestational diabetes mellitus (GDM) Current GDM Past GDM Type 1 or 2 diabetes Nondiabetes Total
No. 81 11 70 70 4339 4490
Periodontitis (%) (Standard error)
OR (95% CI)
Adjusted OR* (95% CI)
29.1 (9.89)
2.54 (0.94-6.86)
2.00 (0.65-6.20)
44.8 25.0 40.3 13.9 14.4
5.33 2.07 4.18 1.00 –
(23.4) (10.18) (9.76) (1.14) (1.19)
(1.08-26.3)y (0.67-6.37) (1.93-9.07) (ref.)
9.11 1.54 2.76 1.00 –
(1.11-74.9)z (0.42-5.59) (1.03-7.35)z (ref.)
OR, Odds ratio; CI, confidence interval. * Adjusted for race/ethnicity, age, marital status, smoking, years of school, and time elapsing since last dental visit. y Compared to 245 nondiabetic pregnant women with prevalence of 13.2% periodontitis. z P ! .05.
In pregnant women, the prevalence of periodontitis was 44.8% in women with GDM and 13.2% in nondiabetic women, with OR of 5.33 (95% CI 1.08-26.3). After adjusting for race/ethnicity, age, marital status, smoking, years of school, and time elapsed since last dental visit, the adjusted odds ratio (aOR) was 9.11 (1.11-74.9). In nonpregnant women, the prevalence of periodontitis was 40.3% in women with type 1 or 2 diabetes, 25.0% in women with previous history of GDM and 13.9% in nondiabetic women, respectively. The ORs were 4.18 (1.93-9.07) for women with type 1 or 2 diabetes, and 2.07 (0.67-6.37) for women with past history of GDM as compared to nondiabetic women. After adjusting for the confounding variables described above, the aORs were 2.76 (1.03-7.35) for women with type 1 or 2 diabetes, and 1.54 (0.42-5.59) for women with past history of GDM.
Comment We are not aware of any previous study reporting an association between periodontal disease and GDM. Our study shows that periodontal disease is associated with GDM in pregnant women as well as type 1 or 2 diabetes in nonpregnant women. Our findings of a high prevalence of periodontal disease in type 1 or 2 diabetics compared to healthy controls in nonpregnant women are consistent with other reports.9 Periodontitis has been referred to as the sixth complication of diabetes13 and has been attributed to consequences of long duration of elevated blood glucose levels (hyperglycemia).14 Impaired insulin resistance, vascular changes, altered oral microflora, abnormal collagen metabolism, and the consequent hyperglycemia and hyperlipidemia of diabetes result in metabolic alterations, which then exacerbate the bacteria-induced inflammatory periodontitis.9,13 A higher prevalence of periodontal disease was found in pregnant women with GDM compared to nondiabetic pregnant women. Pregnancy itself increases gingival
inflammation.15 We cannot rule out that GDM, likewise type 1 or 2 diabetes, may cause periodontitis. However, compared to type 1 or 2 diabetes, GDM represents an early stage of glucose dysregulation and a temporary impaired glucose tolerance that occur in later pregnancy. The elevated glucose levels in the majority of women diagnosed with GDM will usually return to normal after birth.16 Therefore, the hyperglycemia of GDM may be too mild and of too short a duration to have a significant effect on gingival tissues and to cause periodontitis. An alternative explanation is that periodontal disease may be a cause, instead of the result, of GDM. Periodontal infection, a local and chronic subclinical inflammation, induces local and host immune responses and is able to cause transient bacteremia that has impacts on systemic health.6,8 Bacteria from the subgingival plaque and products from the inflamed periodontal tissues (eg, endotoxin: lipopolysaccharide; and inflammatory cytokines: interleukin [IL]-1 and tumor necrosis factor [TNF]-a) enter the circulation and trigger or exacerbate a maternal systemic inflammatory response. It is known that pancreatic b-cell destruction can result from the proinflammatory imbalance created by sustained elevation of IL-1 and TNF-a levels.17 It is well accepted that infection results in a state of insulin resistance.18 Pregnancy itself is a stressful state with increased inflammatory activity19 and marked insulin resistance.20 Therefore, an infection-induced insulin resistance in response to chronic periodontal infection may exacerbate the preexisting pregnancy-induced insulin resistance that may cause impaired glucose tolerance and the manifestation of GDM. Finally, it is possible that the observed association between periodontal disease and GDM might be explained by a common genetic cause for both disorders. Although there is lack of clear correlation between gene polymorphisms and GDM,16 a few studies implicated that polymorphism of cytokines such as TNF-a and IL-1 may be associated with higher risk for insulin resistance or type 2 diabetes,21 as well as periodontal infection.22
Xiong et al There is thus the possibility that preexisting genetic polymorphisms may result in imbalances between the proversus anti-inflammatory cytokine systems predisposing to both periodontal disease and GDM simultaneously. Nonpregnant women who had GDM during previous pregnancies showed an increased prevalence of periodontitis compared to nondiabetics. Since women with GDM are at higher risk of developing type 2 diabetes3 and periodontal disease has been implicated as a risk factor for type 2 diabetes,9,23 this increased prevalence of periodontitis among women with a previous history of GDM observed in the present study may contribute to the development of type 2 diabetes later in life. Several limitations of this study must be pointed out. First, the sample size of the GDM population in the NHANES III survey was small. This was especially true for women with GDM in the current pregnancy, which resulted in imprecise estimates of ORs. Second, data were self-reported, which can result in recall bias. However, several studies have shown that self-reported information on diabetes status as well as sociodemographic characteristics in surveys have a good reproducibility and validity.24 Third, pregnant women who reported GDM in the current pregnancy could have had GDM in a past pregnancy. We cannot exclude those women who had past GDM in current pregnancy from analysis. However, it is noteworthy that women with a previous history of GDM are more likely to have GDM in a subsequent or current pregnancy.1 Because of these limitations, further studies are needed to examine if periodontal disease is an independent risk factor for GDM. Long-term follow-up studies are also needed to test the hypothesis that periodontal disease may contribute to those women with GDM who develop type 2 diabetes later in life. Diabetes, especially type 2, has become one of the most common chronic diseases in the US.25 A large percentage of women with GDM will develop type 2 diabetes later in life.3 GDM provides a window of opportunity for early interventions to prevent later development of type 2 diabetes in young women. Periodontal disease is preventable and curable. If periodontal disease is confirmed as a risk factor for GDM in future studies, this will open the doors to intervention studies. Improving oral health and treating periodontal disease before or during pregnancy may not only reduce maternal and infant morbidity associated with GDM during pregnancy, but also prevent type 2 diabetes later in life. In conclusion, there may be an association between periodontal disease and GDM. Further prospective studies with sufficient sample size are needed for confirmation.
1089
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22. 23. 24.
References 1. ACOG Practice Bulletin. Clinical management guidelines for obstetrician-gynecologists. No. 30, September 2001 (replaces
25.
Technical Bulletin No. 200, December 1994). Gestational diabetes. Obstet Gynecol 2001;98:525-38. Xiong X, Saunders LD, Wang FL, Demianczuk NN. Gestational diabetes mellitus: prevalence, risk factors, maternal and infant outcomes. Int J Gynaecol Obstet 2001;75:221-8. Kim C, Newton KM, Knopp RH. Gestational diabetes and the incidence of type 2 diabetes: a systematic review. Diabetes Care 2002;25:1862-8. Crowther CA, Hiller JE, Moss JR, McPhee AJ, Jeffries WS, Robinson JS. Effect of treatment of gestational diabetes mellitus on pregnancy outcomes. N Engl J Med 2005;352:2477-86. Albandar JM, Rams TE. Global epidemiology of periodontal diseases: an overview. Periodontol 2000 2002;29:7-10. Xiong X, Buekens P, Fraser W, Beck J, Offenbacher S. Periodontal disease and adverse pregnancy outcomes: a systematic review. BJOG 2006;113:135-43. Kinane DF. Causation and pathogenesis of periodontal disease. Periodontol 2000;25:8-20. Garcia RI, Henshaw MM, Krall EA. Relationship between periodontal disease and systemic health. Periodontol 2000;25:21-36. Soskolne WA, Klinger A. The relationship between periodontal diseases and diabetes: an overview. Ann Periodontol 2001;6: 91-8. Plan and operation of the Third National Health and Nutrition Examination Survey, 1988-94. Series 1: programs and collection procedures. Vital Health Stat 1 1994;1-407. Carlos JP, Wolfe MD, 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. Research Triangle Institute: SUDAAN Software for the Statistical Analyses of Correlated Data, SAS-Callable SUDAAN. Version 9.0. NC: Research Triangle Park: Research Triangle Institute, 2004. Loe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993;16:329-34. Matthews DC. The relationship between diabetes and periodontal disease. J Can Dent Assoc 2002;68:161-4. Sooriyamoorthy M, Gower DB. Hormonal influences on gingival tissue: relationship to periodontal disease. J Clin Periodontol 1989; 16:201-8. Buchanan TA, Xiang AH. Gestational diabetes mellitus. J Clin Invest 2005;115:485-91. Moller DE. Potential role of TNF-alpha in the pathogenesis of insulin resistance and type 2 diabetes. Trends Endocrinol Metab 2000;11:212-7. Agwunobi AO, Reid C, Maycock P, Little RA, Carlson GL. Insulin resistance and substrate utilization in human endotoxemia. J Clin Endocrinol Metab 2000;85:3770-8. Redman CW, Sacks GP, Sargent IL. Preeclampsia: an excessive maternal inflammatory response to pregnancy. Am J Obstet Gynecol 1999;180:499-506. Williams D. Pregnancy: a stress test for life. Curr Opin Obstet Gynecol 2003;15:465-71. Tsiavou A, Hatziagelaki E, Chaidaroglou A, Manginas A, Koniavitou K, Degiannis D, et al. TNF-alpha, TGF-beta1, IL-10, IL-6, gene polymorphisms in latent autoimmune diabetes of adults (LADA) and type 2 diabetes mellitus. J Clin Immunol 2004;24:591-9. Kinane DF, Hart TC. Genes and gene polymorphisms associated with periodontal disease. Crit Rev Oral Biol Med 2003;14:430-49. Amar S, Han X. The impact of periodontal infection on systemic diseases. Med Sci Monit 2003;9:RA291-9. Bowlin SJ, Morrill BD, Nafziger AN, Lewis C, Pearson TA. Reliability and changes in validity of self-reported cardiovascular disease risk factors using dual response: the behavioral risk factor survey. J Clin Epidemiol 1996;49:511-7. Harris MI. Diabetes in America: epidemiology and scope of the problem. Diabetes Care 1998;21(Suppl 3):C11-4.
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Periodontal disease and gestational diabetes mellitus Xu Xiong, MD, DrPH,a,* Pierre Buekens, MD, PhD,a Sotirios Vastardis, DDS, MS,b Gabriella Pridjian, MDc Department of Epidemiology,a Tulane University; Department of Periodontics,b Louisiana State University; Department of Obstetrics and Gynecology,c Tulane University, New Orleans, LA Received for publication March 1, 2006; revised May 31, 2006; accepted June 9, 2006
KEY WORDS Diabetes Gestational diabetes mellitus Periodontal disease
Objective: We examined the relationship between periodontal disease and different types of diabetes in pregnant and nonpregnant women. Study design: This study was based on the data from the third National Health and Nutrition Examination Survey (NHANES III), including 256 pregnant and 4234 nonpregnant women. Women were classified into those with gestational diabetes mellitus (GDM) in current pregnancy, with GDM in previous pregnancy, and with type 1 or 2 diabetes. Results: In pregnant women, the prevalence of periodontitis was 44.8% in women with GDM and 13.2% in nondiabetic women, with adjusted odds ratio (aOR) of 9.11 (95% confidence interval [CI] 1.11-74.9). In nonpregnant women, the prevalence of periodontitis was 40.3% in women with type 1 or 2 diabetes, 25.0% in women with previous history of GDM, and 13.9% in nondiabetic women, with aOR of 2.76 (1.03-7.35) for women with type 1 or 2 diabetes. Conclusion: We found an association between periodontal disease and GDM. Ó 2006 Mosby, Inc. All rights reserved.
Gestational diabetes mellitus (GDM) is carbohydrate intolerance with onset or first detection during pregnancy.1 Although there is still debate on the need of universal screening of pregnant women for GDM, GDM is associated with significantly increased risks of maternal and infant morbidity, including macrosomia, preeclampsia, preterm birth, shoulder dystocia, birth injury, and need for cesarean section.1,2 Women with GDM are at a significantly higher risk of developing type 2
Presented at the Twenty-Sixth Annual Meeting of the Society for Maternal Fetal Medicine, Miami, FL, January 30-February 4, 2006. * Reprint requests: Dr Xu Xiong, Department of Epidemiology, School of Public Health and Tropical Medicine, Tulane University, New Orleans, LA 70112. E-mail: [email protected] 0002-9378/$ - see front matter Ó 2006 Mosby, Inc. All rights reserved. doi:10.1016/j.ajog.2006.06.035
diabetes later in life.3 A recent randomized controlled clinical trial has suggested that treatment of GDM reduces serious perinatal morbidity and mortality.4 This was the first large clinical trial that provided evidence to support the use of screening and treatment for women with GDM. Periodontal disease is one of the most common chronic disorders of infectious origin known in humans. The reported prevalence in adults varies between 10% and 60%, depending on diagnostic criteria.5,6 Periodontal disease refers to an inflammatory condition of the soft tissues surrounding the teeth (ie, gingivitis) and the destruction of the supporting structures of the teeth, including the periodontal ligament, bone, cementum, and soft tissues (ie, periodontitis).7 There is increasing evidence suggesting that periodontal disease is
Xiong et al associated with an increased risk of systemic diseases such as cardiovascular diseases, diabetes mellitus, and adverse pregnancy outcomes.6,8 The association between periodontal disease and type 1 or 2 diabetes has been well established. Studies have found not only that type 1 or 2 diabetes increases the risk of developing periodontal disease; periodontal disease may also increase the risk for type 1 or 2 diabetes.9 However, based on our recent systematic review,6 no study has examined the relationship between periodontal disease and gestational diabetes mellitus (GDM). The objective of this study was to examine the relationship between periodontal disease and GDM in pregnant women and type 1 or 2 diabetes in nonpregnant women of childbearing age between 15 and 44 years.
Material and methods Population The study population was a sample from the third National Health and Nutrition Examination Survey (NHANES III). NHANES III was a nationally representative cross-sectional survey of the US civilian, noninstitutional population between 1988 and 1994. A detailed description of the plan and operation of NHANES III has been given elsewhere.10 Because our main interest was GDM and its association with periodontal disease, the data included for this analysis were restricted to women who reported to be pregnant during the survey and women who were of childbearing age between 15 and 44 years. In the NHANES III sample, there were a total of 5317 women who were aged between 15 and 44 years. Among them, 290 women were self-reported to be pregnant at the time of survey. After excluding women who did not complete a periodontal examination (419), or did not have information of diabetes status (361), or had both of these conditions (47), the present study sample included 256 pregnant women and 4234 nonpregnant women aged 15 to 44 years.
1087 standard for periodontal disease diagnosis. In most previous studies, definitions that combined PD and CAL over a certain threshold have been used.6 For this study, periodontal disease (ie, periodontitis) was defined as at least 1 site with CAL or PD R4 mm.11 The independent variables of interest were pregnancy and diabetes status. Pregnancy status was determined based on the question of whether women were pregnant at the time of survey. Diagnosis of diabetes was made from the questions of whether women had ever been told by a doctor or other health professional that they had diabetes; whether the diagnosis had been made during pregnancy; and furthermore, whether they had also been told after or outside of pregnancy that they had diabetes. Based on self-reported diabetes status, women were classified into those with type 1 or 2, with GDM in the current pregnancy and with GDM in a previous pregnancy. The main covariates included race/ ethnicity (defined as non-Hispanic black, non-Hispanic white, and Mexican American), age at interview (recoded as !20, 20-35, O35 years old), marital status (married, single, divorced, widowed), years of education (!12 years, R12 years), smoking status (current smoker, former smoker, never smoker), and time elapsed since last dental visit (%6 months, O6 months, R1 year).
Statistical analyses Univariate analysis was performed to compare the difference in prevalence of periodontal disease between the different types of diabetes and nondiabetic groups according to pregnant and nonpregnant status. Odds ratios (OR) and 95% confidence interval (CI) were calculated. Multivariate logistic regression was performed to further examine the association between periodontal disease and the different types of diabetes, adjusting for age, race/ethnicity, smoking, education, and other confounding variables. Because of the complex survey design used in NHANES III, all analyses were conducted by using the software SUDAAN,12 which provided unbiased standard error estimates by taking into consideration the sampling weights provided in the data set.
Study variables Diagnosis and assessment of periodontal disease is based on clinical criteria. The amount of tissue destruction in periodontitis can be measured by the clinical attachment level (CAL, the distance between the cemento-enamel junction and the apical part of the pocket) and probing depth (PD, the distance from the gingival margin to the apical part of the pocket), using a periodontal probe. In NHANES III, oral health examinations were conducted in mobile examination centers by trained and calibrated dental examiners.10 A maximum of 14 teeth and 28 sites were examined for each participant. There is no universally accepted
Results The Table presents prevalence of periodontitis in pregnant and nonpregnant women with and without different types of diabetes. Overall, among 4490 women aged 15 to 44 years, 75.9% of them were white, 16.8% were black, and 7.3% were Mexican and of other origin; 70% were married, and 33.7% smoked (18.5% for pregnant women). Among the study sample, 81 (1.8%) women had GDM in current or previous pregnancies; 70 (1.6%) had type 1 or 2 diabetes. Among 256 pregnant women, 11 had GDM (4.3%).
1088 Table
Xiong et al Periodontal disease and diabetes in pregnant and nonpregnant women, based on NHANES III, 1988-1994
Diabetes Gestational diabetes mellitus (GDM) Current GDM Past GDM Type 1 or 2 diabetes Nondiabetes Total
No. 81 11 70 70 4339 4490
Periodontitis (%) (Standard error)
OR (95% CI)
Adjusted OR* (95% CI)
29.1 (9.89)
2.54 (0.94-6.86)
2.00 (0.65-6.20)
44.8 25.0 40.3 13.9 14.4
5.33 2.07 4.18 1.00 –
(23.4) (10.18) (9.76) (1.14) (1.19)
(1.08-26.3)y (0.67-6.37) (1.93-9.07) (ref.)
9.11 1.54 2.76 1.00 –
(1.11-74.9)z (0.42-5.59) (1.03-7.35)z (ref.)
OR, Odds ratio; CI, confidence interval. * Adjusted for race/ethnicity, age, marital status, smoking, years of school, and time elapsing since last dental visit. y Compared to 245 nondiabetic pregnant women with prevalence of 13.2% periodontitis. z P ! .05.
In pregnant women, the prevalence of periodontitis was 44.8% in women with GDM and 13.2% in nondiabetic women, with OR of 5.33 (95% CI 1.08-26.3). After adjusting for race/ethnicity, age, marital status, smoking, years of school, and time elapsed since last dental visit, the adjusted odds ratio (aOR) was 9.11 (1.11-74.9). In nonpregnant women, the prevalence of periodontitis was 40.3% in women with type 1 or 2 diabetes, 25.0% in women with previous history of GDM and 13.9% in nondiabetic women, respectively. The ORs were 4.18 (1.93-9.07) for women with type 1 or 2 diabetes, and 2.07 (0.67-6.37) for women with past history of GDM as compared to nondiabetic women. After adjusting for the confounding variables described above, the aORs were 2.76 (1.03-7.35) for women with type 1 or 2 diabetes, and 1.54 (0.42-5.59) for women with past history of GDM.
Comment We are not aware of any previous study reporting an association between periodontal disease and GDM. Our study shows that periodontal disease is associated with GDM in pregnant women as well as type 1 or 2 diabetes in nonpregnant women. Our findings of a high prevalence of periodontal disease in type 1 or 2 diabetics compared to healthy controls in nonpregnant women are consistent with other reports.9 Periodontitis has been referred to as the sixth complication of diabetes13 and has been attributed to consequences of long duration of elevated blood glucose levels (hyperglycemia).14 Impaired insulin resistance, vascular changes, altered oral microflora, abnormal collagen metabolism, and the consequent hyperglycemia and hyperlipidemia of diabetes result in metabolic alterations, which then exacerbate the bacteria-induced inflammatory periodontitis.9,13 A higher prevalence of periodontal disease was found in pregnant women with GDM compared to nondiabetic pregnant women. Pregnancy itself increases gingival
inflammation.15 We cannot rule out that GDM, likewise type 1 or 2 diabetes, may cause periodontitis. However, compared to type 1 or 2 diabetes, GDM represents an early stage of glucose dysregulation and a temporary impaired glucose tolerance that occur in later pregnancy. The elevated glucose levels in the majority of women diagnosed with GDM will usually return to normal after birth.16 Therefore, the hyperglycemia of GDM may be too mild and of too short a duration to have a significant effect on gingival tissues and to cause periodontitis. An alternative explanation is that periodontal disease may be a cause, instead of the result, of GDM. Periodontal infection, a local and chronic subclinical inflammation, induces local and host immune responses and is able to cause transient bacteremia that has impacts on systemic health.6,8 Bacteria from the subgingival plaque and products from the inflamed periodontal tissues (eg, endotoxin: lipopolysaccharide; and inflammatory cytokines: interleukin [IL]-1 and tumor necrosis factor [TNF]-a) enter the circulation and trigger or exacerbate a maternal systemic inflammatory response. It is known that pancreatic b-cell destruction can result from the proinflammatory imbalance created by sustained elevation of IL-1 and TNF-a levels.17 It is well accepted that infection results in a state of insulin resistance.18 Pregnancy itself is a stressful state with increased inflammatory activity19 and marked insulin resistance.20 Therefore, an infection-induced insulin resistance in response to chronic periodontal infection may exacerbate the preexisting pregnancy-induced insulin resistance that may cause impaired glucose tolerance and the manifestation of GDM. Finally, it is possible that the observed association between periodontal disease and GDM might be explained by a common genetic cause for both disorders. Although there is lack of clear correlation between gene polymorphisms and GDM,16 a few studies implicated that polymorphism of cytokines such as TNF-a and IL-1 may be associated with higher risk for insulin resistance or type 2 diabetes,21 as well as periodontal infection.22
Xiong et al There is thus the possibility that preexisting genetic polymorphisms may result in imbalances between the proversus anti-inflammatory cytokine systems predisposing to both periodontal disease and GDM simultaneously. Nonpregnant women who had GDM during previous pregnancies showed an increased prevalence of periodontitis compared to nondiabetics. Since women with GDM are at higher risk of developing type 2 diabetes3 and periodontal disease has been implicated as a risk factor for type 2 diabetes,9,23 this increased prevalence of periodontitis among women with a previous history of GDM observed in the present study may contribute to the development of type 2 diabetes later in life. Several limitations of this study must be pointed out. First, the sample size of the GDM population in the NHANES III survey was small. This was especially true for women with GDM in the current pregnancy, which resulted in imprecise estimates of ORs. Second, data were self-reported, which can result in recall bias. However, several studies have shown that self-reported information on diabetes status as well as sociodemographic characteristics in surveys have a good reproducibility and validity.24 Third, pregnant women who reported GDM in the current pregnancy could have had GDM in a past pregnancy. We cannot exclude those women who had past GDM in current pregnancy from analysis. However, it is noteworthy that women with a previous history of GDM are more likely to have GDM in a subsequent or current pregnancy.1 Because of these limitations, further studies are needed to examine if periodontal disease is an independent risk factor for GDM. Long-term follow-up studies are also needed to test the hypothesis that periodontal disease may contribute to those women with GDM who develop type 2 diabetes later in life. Diabetes, especially type 2, has become one of the most common chronic diseases in the US.25 A large percentage of women with GDM will develop type 2 diabetes later in life.3 GDM provides a window of opportunity for early interventions to prevent later development of type 2 diabetes in young women. Periodontal disease is preventable and curable. If periodontal disease is confirmed as a risk factor for GDM in future studies, this will open the doors to intervention studies. Improving oral health and treating periodontal disease before or during pregnancy may not only reduce maternal and infant morbidity associated with GDM during pregnancy, but also prevent type 2 diabetes later in life. In conclusion, there may be an association between periodontal disease and GDM. Further prospective studies with sufficient sample size are needed for confirmation.
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