Risk factors associated with periodontal disease and its impact on quality of life among pregnant women

Abstract Background Periodontal disease during pregnancy affects maternal oral health and increases the risk of adverse pregnancy outcomes. However, studies on the risk factors for periodontal disease and its impact on oral health-related quality of life in pregnant women in Taiwan are lacking. This present study aimed to identify the risk factors associated with periodontal disease during pregnancy and examine the relationship of periodontal disease with oral health-related quality of life among pregnant women. Methods This study was conducted in a large medical centre in northern Taiwan. Eighty-four participants completed a periodontal examination by dentists as well as structured questionnaires, including the Oral Health Impact Profile-14, demographics, obstetric history, dietary habits, and oral hygiene behaviours. Multivariate logistic regression was used to determine the risk factors associated with periodontal disease and a t-test was used to compare the difference in oral health-related quality of life between pregnant women with and without periodontal disease. Results Fifty participants (59.5%) had periodontal diseases. Risk factors for periodontal disease included eating out for lunch, consuming beverages, brushing less than three times per day, and not receiving regular professional dental cleanings. The oral health-related quality of life was significantly poorer in pregnant women with periodontal disease than in those without. Conclusions The risk factors for periodontal disease, including eating out for lunch, drinking beverages, brushing teeth less, and not regular dental cleaning, provide convincing evidence for pregnant women to maintain good oral hygiene to prevent periodontal disease and improve oral health-related quality of life. PLAIN LANGUAGE SUMMARY Pregnancy can cause poor mouth health. Expectant mothers with gum disease might face problems such as low birth weight and premature birth. This study found that certain factors can worsen gum disease during pregnancy. These include eating out for lunch, drinking sugary or acidic drinks, brushing their teeth less than three daily, and skipping regular teeth cleaning by a dentist. Pregnant women with gum disease also reported a lower quality of life related to oral health compared to those without it. Healthcare providers should educate pregnant women about oral health maintenance. Emphasize the importance of professional dental cleanings every three months, frequent tooth brushing, avoiding sugary and acidic drinks, and reducing eating out for lunch. Future research should explore additional ways to support pregnant women in this regard.

Pregnancy is characterised by physiological changes causing high vulnerability related to oral health.During pregnancy, increases in oestrogen and progesterone levels may result in gingival enlargement, gingival inflammation, and altered subgingival microbiota.Pregnant women with periodontal disease are more susceptible to poor maternal and perinatal outcomes, such as low birth weight (Wang et al. 2013, Mathew et al. 2014), preeclampsia (Khalighinejad et al. 2017), gestational diabetes (Kumar et al. 2018), vulvovaginitis, preterm labour, foetal growth retardation (Figueiredo et al. 2019), and perinatal mortality (Bi et al. 2021).Previous studies have focused on different consequences of increased periodontal disease rates during pregnancy; however, periodontal disease impacts not only pregnancy outcomes but also psychosocial well-being.Pregnant women had more oral complaints, poorer periodontal health and oral health-related quality of life than non-pregnant women (Geevarghese et al. 2017, Adesina et al. 2018).Acharya et al. (2009) assessed the oral health status and related quality of life of 259 pregnant women in India and found that pregnant women with oral problems had poorer oral health-related quality of life.There is limited information on the periodontal conditions of pregnant women in Taiwan, and more comprehensive studies on oral health-related quality of life are necessary.Therefore, the objective of this study was to evaluate the periodontal status of a sample of pregnant women in Taiwan, assess their periodontal condition, measure the prevalence of periodontal disease, and investigate its possible association with sociodemographic factors, habits, oral hygiene, and oral healthrelated quality of life.

Study design
This observational study involved self-report questionnaires and periodontal examinations by dentists.

Participants
The inclusion criteria were as follows: (a) age >20 years, (b) at least 13 gestational weeks, and (c) singleton pregnancy.Participants were excluded if they had one or a combination of the following: risk of preterm labour, antepartum haemorrhage, infection, hypertension, gestational diabetes mellitus, or immunological disease.The sample size was calculated based on a previous study that reported an 84.7% prevalence of periodontal disease during pregnancy and childbearing periods (Wu et al. 2013).A total required sample size of 89 women was calculated using a single population proportion formula considering a 95% confidence interval and 80% power.

Demographics
Demographic information of the participants, including age, education level, marital status, ethnicity, and employment status, were recorded.

Obstetric history
The obstetric history data included gestation, parity, abortions, the last menstrual period, expected date of childbirth, and gestational weeks.

Behaviours or dietary habits
Lifestyle behaviours, including smoking and alcohol consumption before pregnancy, were recorded using yes/no questions.We collected the frequencies of eating out at a restaurant for breakfast/lunch/dinner and grouped them as either more or less than four times per week.Data on intake of beverages, which included any non-alcoholic drinks other than water such as tea, coffee, milk, juice, and soft drinks, among others, were collected and grouped based on frequencies of more or less than three times per week.Data on whether the participants were vegetarian or not were also included.

Oral hygiene behaviours
The oral hygiene behaviours in this study were measured using four yes/no questions during pregnancy, including (1) frequency of teeth brushing grouped into frequencies of more or less than three times per day; (2) using a flossing habit per day; (3) visiting the dentist during pregnancy; and (4) usage of regular professional dental cleaning service every 6 months.

Oral health-related quality of life
The Taiwanese version of the Oral Health Impact Profile-14 (OHIP-14) questionnaire is a reliable (Cronbach's a ¼ 0.90) and valid instrument to measure oral health-related quality of life (OHRQoL) (Kuo et al. 2011).The OHIP-14 questionnaire was developed by Slade (Slade 1997) as a shorter version of the OHIP-49 questionnaire introduced by Locker and Miller (Locker and Miller 1994).The OHIP-14 includes 14 items that explore the following seven conceptual dimensions to measure self-reported frequency of discomfort symptoms: functional limitation, physical pain, psychological discomfort, physical disability, social disability, and perceived handicap (Slade 1997).The responses were measured on a five-point Likert scale and included never (0 points), rarely (1 point), sometimes (2 points), often (3 points), and always (4 points).The higher the OHIP-14 score, the worse the impact on oral health status.In this study, Cronbach's a for the OHIP-14 was 0.90.

Periodontal examination
The examination was performed while the participants sat on a dental chair, with artificial lighting, in the dental unit.An expert dentist conducted the periodontal examinations using a sterilised CP-12 periodontal probe (Hu-Friedy Manufacturing Inc.) and a mouth mirror following the infection-control protocols.Twelve index teeth (11, 14, 16, 21, 24, 26, 31, 34, 36, 41, 44, and 46) were examined.In each sextant, the index teeth were probed at six sites (mesiobuccal, buccal, distobuccal, mesiolingual, lingual, and distolingual).During the examination, the readings or scores were read loudly to research assistants, who simultaneously recorded these scores on a clinical record form with a complete clinical and periodontal description of all the index teeth.
The clinical periodontal parameters included the following: 1) probing depth, 2) clinical attachment level, 3) plaque index and 4) gingival index.The probing depth was measured as the distance in millimetres from the gingival margin to the apical penetration of the probe.The clinical attachment level was calculated based on gingival recession and probing depth measurements and represented the distance from the cemento-enamel junction to the most apical portion of the sulcus/pocket in millimetres.The plaque index (Silness and L€ oe 1964) was used to measure the thickness of the plaque on the gingival one-third and was assigned a score from 0 (no plaque) to 3 (a large amount of plaque) according to the index by Silness and L€ oe.The gingival index, developed by L€ oe, was also used to assess gingivitis (L€ oe 1967).The gingival index was scored as follows: 0 ¼ normal gingiva, 1 ¼ mild inflammation, 2 ¼ moderate inflammation, and 3 ¼ severe inflammation.At the end of the examination, participants were informed of their periodontal status.There are different types of periodontal disease, which include gingivitis and periodontitis.In our study, we used periodontitis to identify the presence of periodontal disease.The criteria used to determine the presence of periodontitis were those established by D€ ortbudak et al, which were at least one site of index teeth with probing depth �5 mm, gingival index �1 mm, and plaque index �1 mm on the same site (D€ ortbudak et al. 2005).

Procedure
This study received ethical approval from the Chang Gung Medical Foundation Institutional Review Board (number: 100-4697A3) and informed consent from all study participants.We used a two-stage process to assess the results of periodontal evaluation and its associations among pregnant women.The first stage of the process consisted of selfadministered and structured questionnaires to collect data on demographics, obstetric history, dietary habits, oral hygiene habits, and OHRQoL.The second stage was carried out in a scheduled dental visit for a comprehensive periodontal examination, which was performed in the same hospital.
Pregnant women attending antenatal check-ups in waiting areas at the outpatient department of the Division of Obstetrics and Gynaecology of Chang Gung Medical Foundation at Linko, a large medical centre in northern Taiwan, were approached by research assistants.Women were provided information about the study if they met the inclusion criteria and did not meet any of the exclusion criteria.The research assistant briefly explained the objectives of the study and procedures involved.Participation was voluntary and would not affect antenatal care in any way.Research assistants obtained informed consent from all participants who voluntarily agreed to participate in the study.In total, 170 pregnant women completed the questionnaire assessment and were then scheduled for one periodontal evaluation 1 -4 weeks after the first-stage assessment.At the second stage, 89 participants attend the periodontal examination.Five participants lost their index teeth and thus do not have full data.Thus, we analysed 84 participants' periodontal status.The reasons for those who did not receive the oral examination were because they were either not available with dental appointments or were no longer pregnant.

Data analysis
Statistical analysis was performed using IBM SPSS software version 28 (IBM SPSS, Armonk, NY, IBM Corp).To test the bivariate relationship between periodontal disease and categorical and continuous variables, the Chi-square and independent t-tests were used, respectively.Variables with a statistically significant association in bivariate analysis were included in the multivariate logistic regression model.Since brushing teeth is the most important variable of oral health, we used multivariable logistic regression to determine whether it was significant or not.Logistic regression analysis was used to examine the effects of various risk factors on periodontal disease.We used Student's t-test to compare the difference in OHRQoL between pregnant women with and without periodontal disease.All factors were analysed with a ¼ 0.05, and p < 0.05 was regarded as significant.

Participant characteristics
This study included 84 participants.Most participants were multipara, in their 2 nd trimester at the time the oral examination was performed, married, employed, at least college graduates, and aged less than 35 years.Fifty participants (59.5%) had periodontal disease.There was no difference in maternal age, advanced maternal age, education, marital status, and employment status between pregnant women with and without periodontal disease (Table 1).Regarding lifestyle behaviours, most women consumed coffee or tea and did not smoke before pregnancy.

Risk factors related to periodontal disease
Regarding dietary behaviour, pregnant women who ate out for lunch more than four times and beverage consumption more than three times per week were more likely to have periodontal disease than those who did not (p ¼ 0.042 and p ¼ 0.004, respectively).Being vegetarian or eating out for breakfast and/or dinner were not significant risk factors for periodontal disease (Table 1).Further, pregnant women receiving regular professional dental cleanings every 6 months were less likely to have periodontal disease (p ¼ 0.019) than pregnant women who did not undergo regular professional dental cleanings.Other oral hygiene behaviours were not significant risk factors for periodontal disease (all p > 0.05).Multivariate logistic regression analysis showed that beverage consumption more than three times per week and eating out for lunch more than four times per week were risk factors for periodontal disease, and brushing teeth more than three times per day and regular professional dental cleaning every 6 months were protective factors for periodontal disease (Table 2).

OHRQoL
The mean OHIP-14 score was 6.26 (SD ¼ 7.60, range 0-39) for all participants.For participants with or without periodontal disease, the mean OHIP-14 scores were 7.35 (SD ¼ 8.60) and 4.64 (SD ¼ 5.53), respectively.There was no significant difference in the mean OHIP-14 scores between the participants with and without periodontal disease.For the OHIP-14 subdimensions, psychological discomfort and handicap were significantly different (p ¼ 0.043 and p ¼ 0.035, respectively).The mean score for psychological discomfort was 1.41 (SD ¼ 1.71) and 0.79 (SD ¼ 1.02) among participants with and without periodontal disease, respectively.The mean score for handicap was 0.57 (SD ¼ 1.17) and 0.18 (SD ¼ 0.39) among participants with and without periodontal disease, respectively.Other sub-dimensions were not different between participants with and without periodontal disease (Table 3).

Discussion
This study contributes to the body of scientific evidence around pregnancy and oral health as the results indicate that pregnant women with a high frequency of eating out for lunch, beverage consumption, not undergoing regular professional dental cleansing, and not brushing their teeth more than three times per day demonstrated a greater prevalence of periodontal disease during pregnancy.Furthermore, pregnant women with periodontal disease had a poorer OHRQoL score, mainly concerning psychological discomfort and handicap dimensions, than pregnant women without periodontal disease.
In the present study, the prevalence of periodontal disease was 59.5%; this finding was higher than those reported in studies conducted in Ethiopia (38.8%) (Belay and Achimano 2022), Sudan (24.0%) (Salih et al. 2020), India (32%) (Singh et al. 2021), and Brazil (47%) (Vogt et al. 2012).In contrast, the prevalence of periodontal disease in our study was found to be lower than that reported by studies from China (84.7%) (Wu et al. 2013) and Italy (61.4%) (Villa et al. 2011).This discrepancy might be due to the different criteria for periodontal disease and research design.We considered the criteria proposed by D€ ortbudak et al. (2005) for periodontal disease in this study because it focuses on the association between periodontal disease and pregnancy outcomes in pregnant women.
Our finding that beverage consumption more than three times per week was significantly associated with periodontal disease highlights the uniqueness of hand-shaken beverages in Taiwan.The culture developed from bubble tea shops that originated in Taiwan in the 1980s.Bubble tea is prepared by mixing tea, syrup, and ice in a shaker.The mixture becomes foamy and the resulting taste and texture are widely popular.These findings were consistent with those reported in previous observational studies that documented the association between high soft drink consumption and periodontal disease in pregnant women (Menezes et al. 2019).
A lifestyle of eating out for lunch more than four times per week during pregnancy was associated with periodontal disease.It is likely that eating out made it harder to maintain regular oral hygiene practices after meals.Teeth brushing is one of the most important oral health behaviours.Previous studies consistently revealed an association between tooth brushing frequency and periodontal disease during pregnancy (Wu et al. 2013, Singh et al. 2021).Our findings indicate that brushing teeth more than three times per day protects against periodontal disease.In terms of professionally performed deep tooth cleaning, our findings indicate that regular dental cleaning every 6 months was a protective factor associated with periodontal conditions.Taiwan's National Health Insurance program is mandatory for all citizens, starting from birth and lasting the entire lifetime.In addition, to enhance oral health during pregnancy, the National Health Insurance provides free dental cleaning for pregnant women every 3 months throughout pregnancy.In our study, 35.8% of pregnant women regularly received professional dental cleaning, a rate higher than that in China (1.2%) (Lu et al. 2015).
This study showed that OHRQoL, as reflected by OHIP-14 scores, was uniformly and significantly poorer among those who had periodontal disease than among those who did not.Although there was no difference in the mean OHIP scores between pregnant women with or without periodontal disease, in the present study, women with periodontal disease reported more psychological discomfort and handicap than those without periodontal disease.However, Lu et al. (2015) evaluated the periodontal health and OHRQoL of 512 pregnant women in China and found a mean OHIP-14 score of 7.92, and multivariable analyses showed that periodontal condition was not significantly associated with OHRQoL.It might be that the different criteria for periodontal disease in the two studies resulted in different impacts on quality of life.The mean OHIP-14 score in the present study was 6.26, which was less than that of pregnant women from China and Brazil (Lu et al. 2015, Caracho et al. 2020).Caracho et al. compared the OHRQoL of pregnant Brazilian women with normal and excess body weight and reported OHRQoL scores of 8.82 and 13.5, respectively (Caracho et al. 2020).The highest impact on OHRQoL was reported in the functional limitation dimension (mean ¼ 0.85) in the present study.In contrast, Lu et al. (2015) reported that physical pain (mean ¼ 1.97) had the highest impact on the OHRQoL.These contrasting findings might be attributed to differences in oral hygiene behaviours and periodontal conditions.
This study is the first to explore the risk factors for periodontal disease and their impact on the OHRQoL of pregnant Taiwanese women.However, it has some limitations.First, the sample size was small owing to the high attrition rate (48%) in the second stage.The second stage included an appointment for periodontal examination.Since most participants were employed (65.1%) or multiparas (58.3%), they did not have time to undergo the periodontal examination.Previous studies used a cross-sectional design to collect questionnaire data and oral examinations simultaneously, and their studies showed a higher response rate (Lu et al. 2015, Belay andAchimano 2022).Second, there is a lack of a gold standard to identify the parameters of oral examination for periodontal disease.It is difficult to compare the prevalence of periodontal disease between different areas and countries.Moreover, we failed to follow up with the participants; hence, the outcomes of the pregnancies were not known.Further research examining the relationship between periodontal disease and perinatal outcomes is needed.
In conclusion, there is a high prevalence of periodontal disease during pregnancy in Taiwan.This study identified the risk factors for periodontal disease during pregnancy, which included eating out for lunch and beverage consumption.The protective factors were brushing teeth more than three times a day and regularly undergoing professional dental cleaning.The findings of the present study have important implications for clinical maternity education and oral health promotion.It is recommended that healthcare professionals provide health education to pregnant women that emphasises the importance of including dental cleansing at least every 3 months, brushing teeth after meals, avoiding beverage consumption, and reducing the frequency of eating out at lunch.

Table 2 .
Risk factors associated with periodontal disease (multivariable logistic regression).

Table 3 .
Differences in Oral health-related quality of life between pregnant women with and without periodontal disease.Student t-test; OHIP: Oral Health Impact Profile..