Prevalence and Risk Factors of Periodontal Disease among Pregnant Women in a Rural Area of China

Background Periodontal disease is one of the most important common oral diseases contributing to the global burden of chronic disease. Systematic reviews have demonstrated that poor periodontal condition during pregnancy was signi�cantly associated with adverse pregnancy outcomes such as preterm birth, low birth weight, preeclampsia, etc. Oral health care is often a neglected area in low-and middle-income countries, particularly in rural areas due to the limited health human resources and poor infrastructures resources. Very few studies have explored the risk factors of periodontal disease among pregnant women in rural areas of China. Methods A cross-sectional study was conducted among 648 women between 2 and 28 weeks of gestation at an antenatal clinic in Maternal and Child Health Hospital of Leping, Jiangxi Province, China. Periodontal Screening & Recording (PSR) was used to determine periodontal disease. Data on respondents’ demographic characteristics, gestational age, regular oral health habits, and mental health condition were collected using a self-administered questionnaire.


Background
Periodontal disease is one of the most important common oral diseases contributing to the global burden of chronic disease.Systematic reviews have demonstrated that poor periodontal condition during pregnancy was signi cantly associated with adverse pregnancy outcomes such as preterm birth, low birth weight, preeclampsia, etc. Oral health care is often a neglected area in low-and middle-income countries, particularly in rural areas due to the limited health human resources and poor infrastructures resources.Very few studies have explored the risk factors of periodontal disease among pregnant women in rural areas of China.

Methods
A cross-sectional study was conducted among 648 women between 2 and 28 weeks of gestation at an antenatal clinic in Maternal and Child Health Hospital of Leping, Jiangxi Province, China.Periodontal Screening & Recording (PSR) was used to determine periodontal disease.Data on respondents' demographic characteristics, gestational age, regular oral health habits, and mental health condition were collected using a self-administered questionnaire.

Conclusions
Pregnant women with increased maternal age and gum bleeding during tooth brushing were at a higher risk of periodontal disease and needed to have the access to oral health care.

Background
Periodontal disease is one of the most important oral diseases contributing to the global burden of chronic disease [1][2][3][4].Globally, more than 75% of adults have oral health problems, such as gingival bleeding, calculus, and shallow or deep periodontal pockets [1].Moreover, 10% to 15% of the adults are with severe periodontal disease [1].According to the ndings of the 3 rd National Oral Health Epidemiological in China, the prevalence of unhealthy periodontal conditions, including gingival bleeding, calculus or periodontal pockets no more than 3mm loss of attachment among Chinese adults was as high as 85% [5].
Oral health care is often a neglected area in low-and middle-income countries, particularly in rural areas due to the limited human resources and poor infrastructures.In 2011, Chinese Ministry of Health released Regulation of Maternal Health Care and Work Speci cation of Maternal Health Care, introducing maternal oral health care into the framework of perinatal health care.However, the oral health care during prenatal care has not been universally provided, especially in underdeveloped rural areas.There is also very few information about oral health conditions and disorders among Chinese rural pregnant women.
Studies have shown factors associated with periodontal disease among general population included the increased age, low educational level, poor economic status, tobacco use, psychological distress, and poor oral hygiene [15][16][17][18][19][20].But very few studies have explored the risk factors of periodontal disease among pregnant women in rural areas of China.
To understand the prevalence of periodontal disease and the risk factors among pregnant women in rural areas of China, we analyze data from the baseline survey of a randomized clinical trial (RCT) in Leping, a rural area of China.

Participants and recruitment
This was the baseline survey of a RCT study which aimed to observe the effects of mouth rinse intervention during pregnancy on reducing the negative pregnancy outcomes such as Premature Rupture of Membranes (PRM), Gestational Diabetes Mellitus (GDM), and Pregnancy-induced Hypertension (PIH) et al [21].The study was conducted in Maternal and Child Health Hospital of Leping, Jiangxi Province, China, a mid-income rural area with around 20% of the total income from agriculture.The hospital is the only maternal and child health care hospital in the county, with a total of 4,000 deliveries annually, accounting for nearly half of the total deliveries in the county.All pregnant women attending prenatal care visits and meeting the criteria were invited to participate in the study by research nurses [21].
The inclusion criteria of participants were as follows: (1) pregnant women who were at least 18 years old with gestational age less than 20 weeks; (2) having an educational level no less than grade 3 in primary school and with the basic ability to read and write; (3) having at least 20 teeth; (4) having no moderate or severe dental caries; (5) having no systemic disease, including severe cardiovascular disease, diabetes, hyperthyroidism, and/or other systemic diseases; (6) having no sexual transmitted disease; (7) willing to participate in the study and to sign the informed consent form.

Research methods and tools
Written informed consent was obtained from each eligible participant before they were provided with a free dental examination for screening periodontal disease.A self-administered questionnaire was distributed, checked and collected by nurses at the recruitment.Ethical approval to conduct this trial has been granted by the Institutional Review Board of School of Public Health, Fudan University, Shanghai, China (IRB# 2013-09-0462); and also by the Institutional Review Board of Tulane University, New Orleans, Louisiana, USA (IRB# 13-469160).The original RCT is registered with Chinese Clinical Trial Registry (#ChiCTR-TRC-13003768) [21].
The self-administered questionnaire mainly contained three sections.Section A was about respondents' demographic characteristics and health related information.Section B collected the information on women's routine oral health habits, including the frequency of daily tooth brushing, the duration of tooth brushing, the habit of rinsing mouth after meals or snacks, and the approach of brushing teeth.Each of four questions about oral health habits was graded with one score.Pregnant women received 0 for none appropriate to four appropriate for all.According to pre-pregnancy BMI, pregnant women were categorized into underweight (£18.5),normal and overweight/obesity (³25).Section C mainly contained a Chinese version of Edinburgh postpartum depression scale (EPDS).It was a 10-item self-report instrument in which women were asked to rate how they had felt in the previous 7 days.EPDS serves as a 'gold standard' for the diagnosis of both Antepartum Depression and Postpartum Depression [22].Each question of EPDS scores 0-3 and the total score ranges from 0 to 30 [22].The increased EPDS scores indicates a higher possibility of antepartum depression.
Dental examination was performed on pregnant women using Periodontal Screening and Recording (PSR) [23].PSR, developed by the American Academy of Periodontology, is a simple, safe, inexpensive and rapid screening tool for periodontal disease compared with the full mouth periodontal examination.During the examination, the mouth was divided into sextants.The dentist examined each sextant by using a ball tipped probe with a color-coded area 3.5mm to 5.5mm.During the examination, the dentist inserted the probe into the periodontal pocket, walked around the circumference of each tooth, observed the position of the color-coded band in relation to the gingival margin, and recorded the highest code of the sextant [23][24][25].Measurements were recorded in a special box chart with 6 blanks to be lled with 6 codes scored 0-4.Code 0 means healthy periodontal conditions with no bleeding after gentle probing and no calculus or defective margins detected; Code 1 means gingival bleeding, which is with bleeding after gentle probing and no calculus or defective margins detected; Code 2 means gingival bleeding and calculus, which is detection of supragingival or subgingival calculus and/or defective margins; Code 3 means shallow periodontal pockets with a probing depth greater than 3.5mm and not more than 5.5mm, de ned as Mild & Moderate Periodontal Disease; Code 4 means deep periodontal pockets with a probing depth greater than 5.5mm, also being de ned as Severe Periodontal Disease [23].Pregnant women were diagnosed with periodontal disease with at least one code higher than 2.

Statistical analyses
analyses were rstly applied to explore the factors associated with periodontal disease, gingival bleeding or calculus, and severe periodontal disease among pregnant women, respectively.Categorical variables were compared using Pearson χ 2 test or Fisher's exact test; Mann-Whitney U test was used for comparing distributions and trends for non-normal distributed data, and also for ordered categorical variables.Finally, multivariable logistic regression model was used to identify factors associated with periodontal conditions.Adjusted odds ratios (aOR) and 95% con dence interval (CI) were derived from the coe cients of the logistic models and their standard errors.The multiple linear regression model was used to test the trend for severity of periodontal disease among pregnant women and risk factors.The severity of periodontal disease was set as an ordinal variable, being coded from one to three representing healthy periodontium, mild/moderate periodontal disease, and severe periodontal disease, respectively.All statistical analyses were performed using SPSS software (SPSS for Windows version 21.0; SPSS Inc., Chicago, IL).
According to trend analysis using the multivariable linear regression, a signi cantly positive linear trend was found between the severity of periodontal morbidity and age, and the trend also was found between the severity and gum bleeding during tooth brushing (Table 3).The severity of periodontal disease advanced with increased ages and gum bleeding during tooth brushing.

Discussion
The study found that periodontal disease was very prevalent, with the prevalence of about 80% among pregnant women in rural china.Among women with periodontal disease, 97% were with mild & moderate periodontal disease and 3% with severe periodontal disease.The increased maternal age and gum bleeding during tooth brushing were associated with an increased risk of periodontal disease.
The prevalence of periodontal disease among rural pregnant women in our study was a bit higher compared with the pre-conception women in an urban area of China (73.9%, 95%CI: 71.0%~76.6%).This might be due to the time of periodontal examination.Estrogen and progesterone, the main hormones during pregnancy, play a signi cant role in aggravating the periodontal disease during pregnancy.As the hormones are continuously produced by corpus luteum after the implantation of a fertilized ovum and to peak in the blood during the third trimester of pregnancy, the periodontal condition usually gets worse with the increased gestation age.
Compared with the other studies conducted among Chinese pregnant women in which the prevalence of gingivitis and periodontitis were showed from 25.5% to 74.8% among pregnant women, the prevalence of our study was higher.The locations of those studies, however, were from the tertiary hospitals in urban cities; whereas the participants in our study were from underdeveloped rural areas, with relatively lower education level and poorer oral health habit.Compared to the United States' prevalence rate (about 24% in adults 30 to 34 years age in NHANES 2009 and 2010), the high prevalence of periodontal disease among rural pregnant women may be due to the fact that oral health care is not well available in China, especially in those less developed areas.
Periodontal disease was considered to be associated with the increased age, overweight, obesity, poor oral hygiene, stressful psychological status, tobacco use, alcohol consumption, taking oral contraceptives, increased parity, and gestational age and so on.In our study, although we have examined a wide range of possible risk factors, the ndings only showed increased age and self-reported gum bleeding during tooth-brushing were associated with periodontal disease.This might be due to the high homogeneity of the study population.Most of the participants shared similar educational background, e.g.most of them with education no more than junior high school, most of their BMI being normal, the similar family income, gestational weeks, EPDS scores, and rare smoking behaviors.
Our ndings are consistent with the prior reports that increased age was a risk factor of periodontal disease [26,27].Similar to another study [28], our study indicated that bleeding during tooth-brushing was signi cantly associated with periodontal disease.This nding suggested that, under the conditions lacking of routine oral health care, a sign of bleeding during tooth-brushing could be regarded as a risky indicator of periodontal disease, and the need of seeking for oral health care.
This study was one of very few ones to explore the factors associated with periodontal disease during pregnancy in rural areas of developing countries.The study showed PSR could be used as a simple, safe and rapid tool for detecting periodontal disease among pregnant women in rural areas.
As the study was the baseline survey of a RCT study, focusing on the periodontal disease and its association with pregnancy outcomes, women with several diseases such as moderate or severe dental caries, some systemic diseases, and sexual transmitted disease were excluded as a way of controlling for confounding factors.Therefore, the ndings of this study may have the limitation of generalizability, and are more likely to be representative for healthy pregnant women.In addition, since the study was conducted in one hospital the generalizability of the ndings might be limited.Due to cross-sectional design, the causal effect cannot be identi ed between the risk factors and periodontal disease.Furthermore, factors included in the study might not be adequate, e.g.dietary information.

Conclusion
A high prevalence of periodontal disease was found among pregnant women in a rural area of China.Advanced maternal age and gum bleeding during tooth brushing were found to be associated with an increased risk of periodontal disease during pregnancy.The sign of gum bleeding during tooth-brushing might suggest the need of seeking for further oral health care.