Individualized Oral Health Education Improves Oral Hygiene Compliance and Clinical Outcomes in Pregnant Women with Gingivitis

Maria L Geisinger^1*, Michelle Robinson², Maninder Kaur³, Robert W Gerlach⁴, Russell Griffin⁵, Nicolaas C Geurs⁶ and Michael S Reddy⁷

¹Department of Periodontology, University of Alabama, Birmingham, USA

²Health Information and Business Systems, University of Alabama, Birmingham, USA

³BDS, MPH, Postdoctoral resident and graduate student, University of Alabama, Birmingham, USA

⁴Research Fellow and Professor, the Proctor and Gamble Company, USA

⁵Department of Epidemiology, University of Alabama, Birmingham, USA

⁶Department of Periodontology, University of Alabama, Birmingham, USA

⁷Professor of Periodontology and Dean, University of Alabama at Birmingham, USA

*Corresponding Author:

Maria L Geisinger
Department of Periodontology
University of Alabama at Birmingham
School of Dentistry, SDB 412
3201 1^st Avenue North
Birmingham, AL 35294-007, USA
Tel: (205) 934-4984
Fax: (205) 934-7901
E-mail: miagdds@uab.edu

Received Date: July 19, 2013; Accepted Date: August 17, 2013; Published Date: August 23, 2013

Citation: Geisinger ML, Robinson M, Kaur M, Gerlach RW, Griffin R, et al. (2013) Individualized Oral Health Education Improves Oral Hygiene Compliance and Clinical Outcomes in Pregnant Women with Gingivitis. J Oral Hyg Health 1:111. doi:10.4172/2332-0702.1000111

Copyright: © 2013 Geisinger ML, et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

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Abstract

Background: Pregnant women have been shown to demonstrate an increase in clinical signs and symptoms of gingivitis despite similar plaque levels to non-pregnant peers. Objective: The goal of this investigation was to utilize a comprehensive regimen of oral hygiene techniques and practices and to evaluate the methodology to teach that regimen by assessing periodontal health outcomes and health behaviors and knowledge in pregnant women. Methods: 120 pregnant participants with Gingival Index (GI) scores ≥ 2 at ≥ 50 % of tooth sites were recruited. At baseline, patients were examined and Plaque Index (PI), Gingival Index (GI), Probing Depth (PD) and Clinical Attachment Level (CAL) were recorded. Patients’ self-reported oral hygiene compliance and oral hygiene knowledge was examined using a pre- and post-test examination at baseline and after the study period. Intensive oral hygiene counseling was provided at baseline, 4 and 8 week visits. Clinical measures and tests of oral hygiene compliance and knowledge were repeated at follow up. Results: A statistically significant reduction in all clinical parameters was shown over the study period. On average whole mouth PI and GI scores were reduced by 54.7% and 48.4%, respectively, and the percentage of sites with PI and GI ≥ 2 decreased from 40% to 17% and 53% to 21.8%, respectively. Whole mouth PD also decreased an average of 0.45 mm and whole mouth CAL decreased an average of 0.24 mm. A statistically significant proportion of patients self-reported an increase in frequency of oral hygiene procedures and an increase in the use of all materials provided in the study oral care regimen. A greater proportion of patients also demonstrated increased knowledge regarding dental and maternal/fetal health after the intervention. Conclusion: Pregnancy may represent a unique opportunity for oral hygiene intervention.

Keywords

Oral hygiene; Pregnancy; Gingivitis; Inflammation; Behavior modification; Periodontal diseases

Introduction

Pregnancy Gingivitis is the most common form of periodontal disease in pregnant women and was extensively described by Loe and Silness [1]. An increase in gingival inflammation throughout pregnancy independent of bacterial plaque accumulation and a return to baseline levels postpartum is seen. The severity of gingival inflammation has been correlated with sex steroid hormone levels during pregnancy [2-4]. The dose-dependent influence of female sex hormone secretion on inflammation increases to high levels from 16-40 weeks and then decreases after parturition. Cross-sectional and cohort studies have demonstrated increased prevalence and severity of gingivitis in pregnant women compared to their non-pregnant female controls, despite similar plaque scores [5,6]. In addition, recent studies indicate that, in the absence of intervention, GI levels and/or Bleeding Upon Probing (BOP) increased into the second trimester and remained elevated until parturition [7,8]. In pregnant patients, altered immunoreactivity to putative periodontal pathogens during pregnancy has been found [7,9]. In healthy individuals a meticulous regimen of daily plaque removal can prevent the onset of gingivitis. In the absence of oral hygiene measures, all individuals develop gingivitis and effective oral hygiene can affect a cure [10]. An intensive approach to plaque removal may be effective to treat pregnancy gingivitis.

Traditionally, the Health Belief Model (HBM), proposed by Hochbaum [11], has been used to alter patients’ oral health behaviors by supplying information allowing patients to make more informed health decisions. A limitation of this approach is that while crosssectional data demonstrate that patients with improved health behaviors also demonstrate high HBM stage [12], longitudinal data do not demonstrate predictive value for behavioral change in patients following presentation of HBM principles [13]. Improvement in knowledge alone may not be adequate to induce behavioral changes. Individualized interventions that establish behaviors as consistent and normative improve success rates in behavior change [14,15]. These practices have been used effectively to improve smoking cessation outcomes in pregnant patients. Smoking cessation has been positively correlated to the patient’s belief that changes in their behaviors will positively affect outcomes in maternal and fetal health [16].

Improving maternal oral hygiene is important for oral health and may reduce systemic pro-inflammatory cytokines and improve maternity outcomes [17,18]. Additionally, children of mothers with optimal oral hygiene habits and knowledge demonstrate lower risk for dental caries [19]. Improving maternal oral health behaviors, therefore, is an important public health issue for women, neonates and children.

This study sought to examine if an intensive oral hygiene regimen focused on pregnancy and maternal/fetal health would reduce the progression of gingivitis during pregnancy and improve patients’ oral health knowledge and perception of oral hygiene importance. The goal was to utilize a comprehensive regimen of oral hygiene techniques and practices and to evaluate the methodology to teach that regimen by assessing periodontal health outcomes and health behaviors and knowledge in pregnant women.

Materials and Methods

Sample size calculation

Prior to initiating this study a sample size calculation was completed. Using data from a previous study [18] and assuming at baseline an average of 60% of sites with either BOP or GI=2, using 80% power the sample size to demonstrate a 33% reduction in whole mouth GI would be 107, well below the reduction seen in the previous study [18].

Enrollment criteria

120 pregnant women between 16 and 24 weeks of gestation established by ultrasound were recruited for participation from the Center for Women’s Reproductive Health (CWRH), University of Alabama at Birmingham (UAB). All study participants were required to present with generalized, moderate to severe gingival inflammation (GI ≥ 2 at 50% of tooth sites) and be free of moderate periodontitis, defined as CAL ≥ 3mm at 3 or more sites, a definition of periodontitis used in a recent large-scale interventional trial, Maternal Oral Care To Reduce Obstetric Risk (MOTOR), examining periodontitis and preterm birth [20]. All patients were ≥ 16 years at enrollment with ≥ 20 natural teeth present. All patients provided informed consent that was approved along with the protocol by the UAB Institutional Review Board.

Baseline visit

After enrollment, patients completed a pre-treatment survey to assess their dental health knowledge and behaviors. The findings of this survey and the follow-up data are detailed in Table 1.

Table 1: Oral Health and Hygiene Habits.

Initial intervention: The participants viewed an educational DVD designed and recorded at UAB at baseline explaining the etiology and disease progression of gingivitis, the potential link between pregnancy gingivitis and prematurity, optimal treatment strategies, as well as a detailed approach to use of the home care aid provided. On the DVD, female dental practitioners presented oral hygiene information and all subjects performing oral hygiene were female. Each participant received a copy of the DVD.

Clinical evaluation: At baseline and all subsequent study visits, a clinical evaluation of each participant’s intra and extra-oral structures was completed by a single examiner (UAB Department of Periodontology) who was trained in study protocol and examination procedures prior to study initiation. Annual retraining sessions were held. Intraexaminer Kappa scores between measurements were 0.962 and 0.884 for PD and CAL, respectively. A clinical cancer screening and examination of the head and neck was performed. The overall level of plaque accumulation and gingival inflammation was recorded per tooth, using Sillnes and Loe indices (PI and GI) [21]. Full-mouth Periodontal Probing Depth (PD), measured from the free gingival margin to the base of the periodontal pocket and attachment (CAL), measured from the Cemento-Enamel Junction (CEJ) to the depth of the periodontal pocket, were recorded to the nearest millimeter with a manual 15mm University of North Carolina (UNC-15) periodontal probe. Each measurement was completed at six sites per tooth (mesiobuccal, buccal, distobuccal, mesiolingual, lingual and distolingual). Sample clinical photographs were obtained of select patient’s dentition to be used as a teaching tool to demonstrating gross plaque, erythema and edema to patients during baseline and treatment visits. A digital SLR camera with a macro-lens and intraoral ring flash were used with a 1:1 magnification.

One-on one intervention: Dental prophylaxis was performed on each patient by the study dentist at the University of Alabama at Birmingham Department of Periodontology using ultrasonic and hand scalers. Topical anesthetic was used to improve patient comfort, if necessary. Individualized one-on-one oral hygiene counseling coupled with demonstration and instructions for using oral hygiene products were completed for each participant. Participants were given an opportunity to ask questions and were asked to demonstrate hygiene techniques until they demonstrated adequate skills and understanding of techniques. An oral health home-care kit was dispensed that was adequate for approximately 6 weeks of use as prescribed. The products included in the home-care kit were selected based upon Cochrane review data demonstrating improved oral hygiene outcomes in patients using an oscillating-rotating mechanical toothbrush compared with manual toothbrushes or other powered or manual toothbrushes [22] and the adjunctive use of flossing as an effective tool in the management of dental caries and periodontal diseases in adults [23]. Furthermore, recent investigations have noted antimicrobial properties of stannous fluoride dentifrice and the efficacy of 0.454% Stannous fluoride dentifrice in reducing gingival inflammation as compared to positive (tricolosan/copolymer) control [24] and the effectiveness of cetyl pyridinium chloride mouthrinse in the reduction of preterm birth rates in a high risk population [25]. Each kit included:

One high-tech powered toothbrush (Oral B Triumph®, Proctor &Gamble Corporation).

0.454% Stannous fluoride toothpaste (Crest Pro Health®).

Dental floss (and interproximal brushes and/or floss-threaders if needed) (Oral B Glide®).

Cetyl pyridinium chloride 0.07% mouth rinse (Crest Pro Health®).

Follow-up intervention: Reinforcement of home care after tooth cleaning was done with periodic cell phone messages, occurring approximately weekly, from the study indicating the importance of oral hygiene during pregnancy.

Visit 2: Participants returned approximately 4 weeks (± 5 days) after baseline in conjunction with an obstetric appointment. Participants updated medical history and any adverse reactions in the mouth recorded. PI and GI were recorded. Based upon clinical findings, oral hygiene instructions were customized and reinforced via repeated counseling and demonstration focusing on areas of plaque retention and gingival inflammation identified in clinical examination. Home care kits were replenished. Subjects did not return empty packaging.

Visit 3: Participants returned approximately 8 weeks (± 5 days) after baseline visit in conjunction with an obstetric appointment. Participants updated medical history and adverse reactions were recorded. Participants completed a post-intervention survey to assess current dental knowledge, attitudes, behavior patterns and their subjective assessment of the study experience. The results of this survey and its comparison to the baseline survey are detailed in Table 1. A comprehensive clinical evaluation was completed identical to the baseline evaluation. Additional oral and baby care products including baby toothbrushes and store coupons were dispensed to participants who completed the study.

Data Analysis

Mixed-model Analysis of Variance (ANOVA) was used to compare measurements of PI, GI, PD and CAL between the baseline and followup examinations, accounting for correlations among measurements made on the same patient and controlling for tooth and surface. Time, tooth, and surface were included as fixed effects in each model and a compound symmetric variance structure was assumed. The maximum value of each measurement across the buccal, lingual, distal and mesial sites on each tooth was used in the analysis. Statistical significance was set at p<0.01 so that the data were comparable to similar experiments in previously published reports. Results are presented as least-squares means and standard errors, in order to account for multiple and unequal numbers of observations per patient. Differences in distributions of responses to survey questions between the initial and follow-up administrations were evaluated using Bowker’s test of symmetry.

Results

120 participants were enrolled, but one participant failed to complete the baseline visit and did not receive any oral hygiene counseling and/ or products. 119 pregnant participants treated with intensive dental prophylaxis and oral hygiene instructions were compared before and 8 weeks after the intervention. No significant adverse reactions were reported after the nonsurgical therapy or to any of the home care aids provided to the patients. Study population demographics are detailed in Table 3. There were no statistically significant differences between subjects who completed all oral hygiene procedures and those who failed to complete all study procedures.

Table 2: Periodontal Measurements at Baseline and 8 Weeks.

Table 3: Study Population Demographics: Comparison between all enrolled subjects (N=119) and those lost to follow up (N=23).

Whole mouth PI significantly reduced from a mean value of 1.35 ± 0.07 at baseline to 0.61 ± 0.07 after intervention. Whole mouth GI was significantly reduced from a mean value of 1.45 ± 0.07 at baseline to 0.75 ± 0.07 at 8 weeks follow-up. Whole mouths mean PD was significantly reduced from 3.41 ± 0.10 mm at baseline to 2.97 ± 0.10 at the 8 week follow-up visit. Whole mouths mean CAL was significantly reduced from 2.26 ± 0.10 mm at baseline to 2.02 ± 0.10 mm at the 8 week follow-up visit (Table 2). A typical clinical response from baseline to 8 weeks post-intervention is illustrated in Figures 1 and 2.

Figure 1: Baseline frontal intraoral photographs.

Figure 2: 8-Week intraoral frontal photographs.

There were statistically significant differences between baseline and post-intervention in the reports of tooth brushing frequency, flossing frequency and mouth rinsing frequency. Patients also reported statistically significant differences in the types of toothpaste and mouth rinse used at baseline and post-intervention. Paralleling the marked decreases in GI, a statistically significant proportion of patients reported decreased frequency of gingival bleeding with oral hygiene measures and also a statistically significantly greater proportion of patients reported that their “gums hurt and bled” post-intervention than did at baseline. There were no statistically significant differences in proportions of patients reporting noticeable bad breath, difficult oral hygiene tasks, or the reasons for difficulty. Six enrolled patients complete oral hygiene interventions, but did not complete the post-test intervention of their choosing. These findings are summarized in Table 1 and Figure 3.

Figure 3: Oral health and Hygiene habits.

Overall after the 8-week study period, patients demonstrated a higher level of knowledge about the possible link between gingivitis and preterm birth. There was a statistically significant increase in the proportion of patients who reported that improved daily oral hygiene could reduce gingivitis after the intervention period when compared to baseline levels. Additionally, a statistically significantly larger portion of the population demonstrated increased knowledge about untreated gingivitis and its affect on maternal and fetal health post-intervention when compared to baseline knowledge levels. A statistically significant proportion of patients also reported that excellent dental hygiene was important for maternal and fetal health after the intervention than at baseline. Six enrolled patients complete oral hygiene interventions, but did not complete the post-test intervention of their choosing. These findings are summarized in Table 4 and Figure 4.

Table 4: Oral Health and Hygiene Knowledge.

Figure 4: Oral Health and Hygiene Knowledge.

Discussion

An increase in the clinical signs and symptoms associated with gingivitis without marked changes in the quantity of bacterial flora has been noted in pregnant females [1]. The levels of female gonadotropins during pregnancy correlate with the severity of gingival diseases. Increased levels of progesterone are associated with increased membrane permeability, which may contribute to vascular permeability and subsequent edema of gingival tissues [26]. Furthermore, increasing salivary levels of estradiol and progesterone have been correlated with a 55-fold increase in the proportion of P. intermedia in the bacterial flora during pregnancy [27,28]. This bacterial shift may be due to the opportunistic substitution by P. intermedia and other Bacteroides spp. of progesterone and estrogen for Vitamin K, and essential growth factor [29]. Estrogen receptors (ERβ) have been identified on gingival epithelium and periodontal ligament [30,31] and the direct effects of pregnancy hormones on periodontal tissues [32] may account for gingival inflammation during pregnancy.

Despite the increased severity of gingival inflammation and qualitative differences in subgingival plaque composition in pregnant females, in the absence of pathologic periodontal pocketing and attachment loss, the condition is usually self-limiting and reversible after parturition and/or lactation when hormone balance is achieved. Since gingivitis and its effects on the periodontium are reversible there is a common misconception that a prolonged state of gingival inflammation during pregnancy does no potential harm. Because women with pregnancy gingivitis demonstrate increased bleeding and gingival crevicular fluid production, the potential for bacteremias and increased serum levels of pro-inflammatory cytokines may make effective treatment of gingivitis during pregnancy important for overall maternal and fetal health.

The combined approach of one-on-one oral hygiene counseling with a dentist or dental hygienist, DVD oral hygiene instruction, dental prophylaxis and a multiproduct oral hygiene regimen was effective in significantly reducing the whole-mouth PI, GI, PD, and CAL values in pregnant patients over an 8-week treatment time. In the absence of intervention, GI levels and/or BOP increase into the second trimester and remain elevated until parturition [6,7]. Despite the elevated hormone levels in these patients due to their progressive gestation [3], the nonsurgical intervention was effective in reducing the patients overall gingivitis levels. This indicates that improved plaque removal is adequate to improve the clinical signs of plaque-induced gingivitis modified by pregnancy. While previous oral health interventions in pregnant patients did include oral hygiene instructions and/or monthly supragingival tooth polishing, [33,34] the regimen of mechanical tooth brushing, floss, alcohol-free mouth rinse, a take-home instructional DVD discussing oral hygiene and its importance and monthly oneon- one oral hygiene instructions may have more effectively decreased pregnancy gingivitis. The statistically significant preference for the multiproduct regimen post-intervention may reflect a positive attitude for the no-cost products provided to participants in the trial.

Use of dental practitioners and oral hygiene demonstrators who closely reflected the patient population may have also improved acceptance of the oral hygiene instruction. Further, since the periodontal care was provided at the Center for Women’s Reproductive Health in conjunction with the subjects prenatal visits the connection between periodontal and fetal/maternal health may have been a more impactful message leading to behavioral changes. Previous data have indicated that patients smoking cessation led by healthcare providers and methods involving individualized care for tobacco cessation were more successful than self-directed care [35,36]. These authors also found that external incentives did not improve cessation outcomes, but awareness of overall health benefits did show positive benefit. Subjects receiving information about oral health in an obstetric environment may have similar attitudes regarding the far-reaching effects of oral health and hygiene.

Success of periodontal therapy is oftentimes dependent upon patient compliance with oral hygiene and maintenance regimen, long-term behavioral changes are necessary and suboptimal patient compliance can compromise ideal results [37,38]. Oral hygiene intervention in pregnant patients allows a practitioner to take advantage of increased motivation due to a novel device (i.e. Hawthorne effect) [39] as only a short term intensive regimen is necessary as the vast majority of cases of pregnancy gingivitis will resolve after parturition without intervention. The effect of such a novel device may have been seen in this case, as the patients were given a powered toothbrush. A further advantage of treating gingivitis in pregnant patients is that unlike other chronic systemic conditions such as Diabetes Mellitus and cardiovascular disease where significant, long-term changes may be necessary to increase periodontal health and positively affect the chronic disease, pregnant patients need only adapt positive health behaviors for a short time frame to potentially have a positive effect on pregnancy outcomes. Of course, behavioral changes in pregnancy have been shown in many cases to translate into long-term alterations in health behaviors, which may have positive impact on the oral and overall health of neonates and children [19].

Success of periodontal therapy is oftentimes dependent upon patient compliance with oral hygiene and maintenance regimen, long-term behavioral changes are necessary and suboptimal patient compliance can compromise ideal results [37,38]. Oral hygiene intervention in pregnant patients allows a practitioner to take advantage of increased motivation due to a novel device (i.e. Hawthorne effect) [39] as only a short term intensive regimen is necessary as the vast majority of cases of pregnancy gingivitis will resolve after parturition without intervention. The effect of such a novel device may have been seen in this case, as the patients were given a powered toothbrush. A further advantage of treating gingivitis in pregnant patients is that unlike other chronic systemic conditions such as Diabetes Mellitus and cardiovascular disease where significant, long-term changes may be necessary to increase periodontal health and positively affect the chronic disease, pregnant patients need only adapt positive health behaviors for a short time frame to potentially have a positive effect on pregnancy outcomes. Of course, behavioral changes in pregnancy have been shown in many cases to translate into long-term alterations in health behaviors, which may have positive impact on the oral and overall health of neonates and children [19].

The self-reported rates of oral hygiene at baseline were similar to previously published levels of oral hygiene frequency in other pregnant populations [40,41] and were slightly below the overall reported rates for frequency of oral hygiene performance in general population studies [42-44]. In this investigation, patients reported statistically significant increased in frequency of tooth brushing, flossing and mouth rinsing. For example, 49% of subjects reported flossing less than once monthly at baseline whereas all subjects reported flossing at least weekly after the intervention and 88% of subjects reported flossing daily. A statistically significantly greater proportion of patients demonstrated correct understanding of the importance of oral hygiene in the prevention of gingivitis and the effect of adequate oral health on overall maternal/ fetal health after the study intervention as compared to baseline levels. These findings may indicate that subjects perceived their oral health to be important to their overall health and that of their fetus, which may have prompted the behavioral changes.

The changes in clinical outcomes indicate patients had a more effective plaque removal regimen after the intervention and the survey data also indicate an improvement in frequency of oral hygiene measures and an improvement in knowledge regarding the importance of oral hygiene to overall health in pregnant patients. Individualized intervention and emphasis of the relationship between oral hygiene and overall health and maternity outcomes may have shifted subject behaviors and attitudes towards hygiene measures in this study. The larger percentage of subjects reporting gingival bleeding may indicate that subjects were more apt to be performing hygiene measures and performing them correctly. This shift in the self reported data may reflect an increase in patient awareness of their oral health and pathologic symptoms of gingivitis.

A limitation of this study design includes the lack of control subjects who were observed, but did not receive oral hygiene instructions. This study design was based upon previous investigations that demonstrated increasing gingival inflammation throughout pregnancy [2], but in future investigations a controlled trial would allow for additional conclusions about the effectiveness about this oral hygiene regimen in pregnant patients and its effect on behavioral changes. It is possible that patients who were examined, but did not receive interventional oral hygiene instructions and oral hygiene products would also demonstrate improvements. Additional larger scale prospective interventional trials are needed to determine the true effect of these interventions on oral health and behavior during pregnancy.

Furthermore, this intervention may be well suited for a widespread public health intervention performed by dental and/or medical auxiliary personnel. Rates of pregnancy gingivitis have been demonstrated to be higher in African American women [45] and those with lower socioeconomic status [46]. In these high-risk populations low cost interventions may result in overall improvement of maternal, fetal and childhood oral and systemic health. Limitations for largescale application of this type of treatment may include cost-benefit analysis of the cost of the study materials and personnel requirements as compared with the economic and health benefits of the intervention on oral health and pregnancy outcomes. Further studies may focus on the feasibility and Cost-Utility Analysis (CUA) [47] of application of these interventions for public health and in clinical practice.

Conclusions

An intensive regimen of repeated and systematic individualized oral hygiene instructions combined with a multiproduct oral hygiene regimen was able to statistically significantly reduce all clinical signs of periodontal and gingival inflammation in pregnant women. Survey data indicate that patients’ knowledge about the etiology and possible systemic effects of gingivitis improved with individualized intervention. Pregnancy may allow a unique opportunity for motivation to change oral hygiene behaviors with an intense, individualized education program.

Acknowledgements

This research was supported in part by funding and materials from the Procter & Gamble Company (Cincinnati OH, USA). Drs. Geisinger, Robinson, Kaur, Griffin, Geurs, and Reddy declare no financial relationships or conflicts of interest related to any products involved in this study. Dr. Gerlach is employed by the Proctor & Gamble Company as a Research Fellow and Professor in the division of Global Oral Care.

Clinicaltrials.gov

NCT00641901

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