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J Clin Periodontol 2014; 41: 141–148 doi: 10.1111/jcpe.

12188

Case Report
Oral health education and Maria L. Geisinger1, Nicolaas C.
Geurs1, Jennifer L. Bain1, Maninder
Kaur1, Philip J. Vassilopoulos1,

therapy reduces gingivitis during Suzanne P. Cliver2, John C. Hauth2


and Michael S. Reddy1
1
Department of Periodontology, School of

pregnancy Dentistry, University of Alabama at


Birmingham, Birmingham, AL, USA;
2
Department of Obstetrics and Gynecology,
School of Medicine, University of Alabama at
Birmingham, Birmingham, AL, USA
Geisinger ML, Geurs NC, Bain JL, Kaur M, Vassilopoulos PJ, Cliver SP, Hauth
JC, Reddy MS. Oral health education and therapy reduces gingivitis during
pregnancy. J Clin Periodontol 2014; 41: 141–148. doi: 10.1111/jcpe.12188.

Abstract
Background: Pregnant women demonstrate increases in gingivitis despite similar Clinicaltrials.gov: NCT00641901
plaque levels to non-pregnant counterparts.
Aim: To evaluate an intensive protocol aimed at reducing gingivitis in pregnant
women and provide pilot data for large-scale randomized controlled trials investi-
gating oral hygiene measures to reduce pregnancy gingivitis and alter maternity
outcomes.
Materials and Methods: One hundred and twenty participants between 16 and
24 weeks gestation with Gingival Index (GI) scores ≥2 at ≥50% of tooth sites
were enrolled. Plaque index (PI), gingival inflammation (GI), probing depth (PD),
and clinical attachment levels (CAL) were recorded at baseline and 8 weeks. Den-
tal prophylaxis was performed at baseline and oral hygiene instructions at base-
line, 4 and 8 weeks. Pregnancy outcomes were recorded at parturition. Mixed-
model analysis of variance was used to compare clinical measurements at baseline
and 8 weeks.
Results: Statistically significant reductions in PI, GI, PD, and CAL occurred over
the study period. Mean whole mouth PI and GI scores decreased approximately
50% and the percentage of sites with PI and GI ≥2 decreased from 40% to 17%
Key words: behaviour modification; gingivitis;
and 53% to 21.8%, respectively. Mean decreases in whole mouth PD and CAL inflammation; oral hygiene; pregnancy;
of 0.45 and 0.24 mm, respectively, were seen. preterm birth
Conclusions: Intensive oral hygiene regimen decreased gingivitis in pregnant
patients. Accepted for publication 20 October 2013

Pregnancy Gingivitis has been exten- Durlacher et al. 1994, Figuero et al. more severe inflammation with simi-
sively described in the literature (L€
oe 2013). Previous work demonstrates a lar levels of etiologic factors (Arafat
& Silness 1963, Mariotti 1994, Raber- progressive increase in gingival 1974, Ness & Perkins 1980, Yalcin
inflammation throughout pregnancy et al. 2002, Gursoy et al. 2008). The
Conflict of interest and source of
independent of bacterial plaque severity of gingival inflammation
funding statement
accumulation and a return to base- observed has been correlated with
Drs. Geisinger, Geurs, Bain, Kaur, line levels postpartum. Plaque- sex steroid hormone levels during
Vassilopoulos, Hauth and Reddy and induced gingivitis is the most com- pregnancy (L€ oe & Silness 1963, Zaki
Ms. Cliver declare no financial rela- mon form of periodontal disease in et al. 1984, Raber-Durlacher et al.
tionships or conflicts of interest pregnant women affecting 36–100% 1993, Figuero et al. 2010). This indi-
related to any products involved in of pregnant subjects (Maier & Orban cates a possible dose-dependent
this study. This research was sup-
1949, L€ oe & Silness 1963, Jansen influence of female sex hormone
ported in part by funding and materi-
et al. 1981). Clinical characteristics secretion on inflammation, which
als from the Procter & Gamble
Corporation (Cincinnati, OH, USA).
of pregnancy-associated gingivitis increases to high levels from 16 to
clearly show a tendency towards 40 weeks and then decreases after
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd 141
142 Geisinger et al.

parturition. Cross-sectional and odontal clinical parameters in preg- Baseline visit


cohort studies have demonstrated nant patients. Initial intervention
increased prevalence and severity of
gingivitis in pregnant women com- The participants viewed an educa-
Materials and Methods tional DVD designed and recorded
pared to their non-pregnant female
controls, despite similar plaque at UAB at baseline, which explained
Sample size calculation
scores (L€oe 1965, Cohen et al. 1971). the potential link between pregnancy
Other reports have demonstrated Prior to initiating this study a sam- gingivitis and prematurity as well as
altered immunoreactivity to putative ple size calculation was completed. a detailed approach to use of the
periodontal pathogens during preg- Using data from a previous study home-care aids provided. Each par-
nancy (Lopatin et al. 1980, Kinny (Lopez et al. 2005) and assuming at ticipant also received a copy of the
et al. 1996). In the absence of oral baseline an average of 60% of sites DVD for further reference at home.
hygiene measures, all individuals with either BOP or GI = 2, using Clinical evaluation
develop gingivitis and in healthy indi- 80% power the sample size to dem-
viduals a meticulous regimen of daily onstrate a 33% reduction in whole At baseline and all subsequent study
plaque removal can prevent the onset mouth GI would be 107 subjects. visits, a clinical evaluation of each
of gingivitis and effective oral hygiene participant’s intra and extra-oral
can affect a cure (L€oe et al. 1965). structures was completed by a cali-
Enrolment criteria brated examiner. A clinical cancer
While treating gingivitis in preg-
nant women is of concern for optimal One hundred and twenty pregnant screening and examination of the
oral health, there is evidence that gin- women between 16 and 24 weeks of head and neck was completed. All
givitis may influence pregnancy out- gestation from the Center for examination procedures were per-
comes, which makes intervention of Women’s Reproductive Health formed by a single examiner (UAB,
interest from a public health stand- (CWRH) at the University of Ala- Department of Periodontology) who
point and gives further weight to bama at Birmingham (UAB) were was trained in study protocol and
affecting a cure (Chambrone et al. recruited to participate in this study. examination procedures prior to
2011a,b). Periodontal disease has All study participants were required study initiation. Annual retraining
been identified as a risk factor for to present with generalized, moder- sessions were held. Intra-examiner
adverse pregnancy outcomes (Jeffcoat ate to severe gingival inflammation Kappa scores between measurements
et al. 2001, Offenbacher et al. 2001), (GI ≥ 2 at ≥ 50% of sites) and be were 0.962 and 0.884 for PD and
but the efficacy of periodontal treat- free of periodontitis, defined as CAL, respectively. The overall level
ment on birth outcomes has been CAL > 3 mm at 3 or more sites, the of plaque accumulation and gingival
inconsistent (Lopez et al. 2005, Mich- definition of periodontitis used in a inflammation was measured per
alowicz et al. 2006, Wimmer & Pihl- recent large-scale interventional trial tooth, using Silness and L€ oe indices
strom 2008, Kunnen et al. 2010, examining periodontitis and preterm (PI and GI; L€ oe 1967). Full-mouth
Chambrone et al. 2011a,b). While birth, Maternal Oral Therapy to periodontal pocket depth (PD), mea-
this study was not powered to demon- Reduce Obstetric Risk (MOTOR) sured from the free gingival margin
strate differences between maternity (Offenbacher et al. 2009), as patients to the base of the periodontal
outcomes, it may allow pilot data for for this intervention were recruited pocket, and attachment (CAL), mea-
future large-scale randomized con- in parallel with those with periodon- sured from the cemento-enamel junc-
trolled trials evaluating the effective- titis enrolled in the aforementioned tion (CEJ) to the depth of the
ness of an intensive home-care large-scale interventional trial using periodontal pocket, were recorded to
regimen on maternity outcomes in the same personnel and facilities. All the nearest millimetre with a manual
women with pregnancy gingivitis. patients were 16 years or older at en- 15 mm University of North Carolina
We hypothesized that gingivitis rolment with a minimum of 20 natu- (UNC-15) periodontal probe. Each
during pregnancy could be con- ral teeth present in the mouth. Prior measurement was completed at six
trolled with a minimally invasive to enrolment, all patients underwent sites per tooth (mesiobuccal, buccal,
approach which used an intensive an informed consent process that distobuccal, mesiolingual, lingual,
oral hygiene regimen and behaviour- was approved along with the proto- and distolingual). Sample clinical
al and educational counselling to col by the UAB Institutional Review photographs were obtained of select
improve home care in pregnant Board. Of the patients recruited, 119 patients dentition to be used as a
patients. Due to the widespread received oral examinations and 117 teaching tool to demonstrate gross
prevalence of pregnancy gingivitis have pregnancy outcome data. plaque, erythema and oedema to
the development of a home-care reg- Patients were recruited between patients during baseline and treatment
imen to reduce gingivitis in pregnant April 2007 and October 2008. Final visits. A digital SLR camera with a
women could be a cost-effective parturition data was obtained in macro-lens and intra-oral ring flash
mechanism to improve the health of February of 2009. Subjects were were used with a 1:1 magnification.
pregnant women. This study evalu- excluded if they had the following One-on-one intervention
ated changes in PI, GI, PD, and risk factors for preterm birth: plural
CAL from baseline to 8-weeks post- gestations, previous spontaneous Dental prophylaxis was performed on
intervention to determine if intensive preterm birth, body mass index each patient by a study periodontist at
oral hygiene instructions and home- <19.8 or bacterial vaginosis as the University of Alabama at Birming-
care regimen could improve peri- assessed by a gram stain. ham Department of Periodontology
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Hygiene regimen for pregnancy gingivitis 143

using ultrasonic instruments and hand recorded. PI and GI were recorded. surements of PI, GI, PD, and CAL
scalers and curettes. Topical anaesthe- Based upon clinical findings and at the between the baseline and follow-up
sia was used to improve patient com- discretion of the study dentist, learning examinations, accounting for corre-
fort, if necessary. If possible, the was reinforced via repeated counselling lations among measurements made
procedures were completed in one ses- and demonstration focusing on areas on the same patient and controlling
sion; however, an additional session of plaque retention and gingival for tooth and surface. Time, tooth,
was scheduled to complete therapy inflammation identified in clinical and surface were included as fixed
based upon overall levels of plaque examination, as is standard of care in effects in each model and a com-
and calculus deposits, time constraints, many clinical practice settings (Rode pound symmetric variance structure
and patient needs as is standard of Sde et al. 2012). Home-care kits were was assumed. The maximum value
care in many periodontal clinical prac- replenished. Subjects did not return of each measurement across the
tice settings (Rode Sde et al. 2012). empty packaging. buccal, lingual, distal and mesial
Individually tailored intensive one-on- sites on each tooth was used in the
one oral hygiene counselling providing Visit 3 analysis. Statistical significance was
feedback regarding both positive and set at p < 0.01 so that the data
negative aspects of oral hygiene perfor- Participants returned 8 weeks were comparable to similar experi-
mance coupled with demonstration (5 days) after baseline visit. Partici- ments in previously published
and instructions for using oral hygiene pants updated medical history and reports.
products (and subsequent visits as any adverse reactions were recorded.
needed) were completed for each par- Intra and extra-oral evaluation,
along with a follow-up comprehen- Results
ticipant. A personal interview was con-
ducted by a study dentist to determine sive clinical evaluation of periodon- One hundred and nineteen pregnant
intra-oral areas and/or oral hygiene tal probing examination, plaque, and participants were treated with dental
techniques about which a patient gingival measurements were com- prophylaxis and intensive oral
reported difficulty. These patient- pleted identical to the baseline evalu- hygiene instructions. No significant
reported factors were coupled with the ation. A follow-up survey was adverse reactions were reported after
study examiner’s findings to develop a administered to determine subjects’ dental prophylaxis or to any of the
comprehensive oral hygiene plan for level of oral hygiene knowledge and home-care aids provided to the
the patient using a multiproduct regi- current oral hygiene regimen, includ- patients. The demographics of the
men. Intraoral photographs of the ing product usage and frequency. study participants are detailed in
patient’s dentition were used to demon- Additional oral and baby care prod- Table 1. Twenty-three patients were
strate gingival inflammation and plaque ucts including baby toothbrushes and lost to follow-up. Patients did not
biofilm deposits to patients. A focus on store coupons were dispensed to par- complete study procedures due to
the patient as a co-practitioner and an ticipants who completed the study. missing prenatal appointments and
emphasis on self-care during pregnancy the oral hygiene appointments sched-
were discussed with each patient as a Pregnancy outcomes uled in conjunction with these prena-
part of this intervention. An oral health tal visits. There were no statistically
A blinded examiner (University of
home-care kit was dispensed that was significant differences between sub-
Alabama, Department of Obstetrics
adequate for approximately 6 weeks of jects who completed all oral hygiene
and Gynecology) recorded gesta-
use as prescribed. Each kit included: procedures and those who failed to
tional age (GA) at the end of preg-
One powered toothbrush (Oral B Tri- complete all study procedures. All
nancy for all participants and these
umphâ; Procter & Gamble, Cincinnati, data were sealed until all enrolled
enrolled subjects were evaluated for
OH, USA); 0.454% Stannous fluoride parturition outcomes. Whole mouth
subjects had reached parturition. GA
toothpaste (Crest Pro Healthâ; Procter was calculated in this study based
plaque index scores were signifi-
& Gamble); Dental floss (and inter- cantly reduced from a mean value of
upon last menstrual period (LMP)
proximal brushes and/or floss-threaders 1.35 (SD = 0.07) at baseline to 0.61
confirmed with ultrasound measure
if needed); Cetyl pyridinium chloride (SD = 0.07) at the 8 week follow-up
at <20 weeks gestation. If LMP and
0.07% mouth rinse (Crest Pro visit. In addition, whole mouth gin-
ultrasound measure did not agree
Healthâ). within 7 days or if the subject did
gival index scores showed a signifi-
cant reduction from a mean value of
Follow-up intervention not have a sure LMP, ultrasound
1.45 (SD = 0.07) at baseline to 0.75
measure was used to determine ges-
Reinforcement of home care after (SD = 0.07) at the 8 week follow-up
tational age. Prematurity was defined
tooth cleaning was done with peri- visit. Whole mouth mean probing
in this study as birth prior to 37
odic cell phone messages from the depths were significantly reduced
completed weeks (259 days) of gesta-
study indicating the importance of from 3.41 mm (SD = 0.10) at base-
tion and prior to 35 complete weeks
oral hygiene during pregnancy. line to 2.97 mm (SD = 0.10) at the
(245 days) of gestation as these GA
8-week follow-up visit. Whole mouth
benchmarks were used in similar
mean clinical attachment levels were
Visit 2 recent studies (Jeffcoat et al. 2011a,b).
also significantly reduced from
Participants returned 4 weeks 2.26 mm (SD = 0.10) at baseline to
Data analysis
(5 days) after baseline. Participants 2.02 mm (SD = 0.10) at the 8 week
updated medical history and any Mixed-model analysis of variance follow-up visit (Table 2). A typical
adverse reaction in the mouth was (ANOVA) was used to compare mea- clinical response from baseline to
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
144 Geisinger et al.

Table 1. Study population demographics


Total enrolled* Enrolled* (loss to follow-up) p-Value
n = 119 (%) n = 23 (%)

Race/Ethnicity
Black 82.5 69.9 0.0838
White, non-hispanic 10.8 26.1
Hispanic/Latino 5.8 0
Other 0.8 4.3
Education level
Less than high school 1.7 4.3 0.2778
High school diploma 70.0 78.3
Some college or college 27.5 13.0
Marital status Fig. 2. Eight-week intra-oral frontal pho-
Married 10.8 13.0 0.7550 tographs demonstrating a typical clinical
Unmarried 88.3 82.6 response to the intensive oral hygiene
Age regimen from 16 to 24 weeks gestation in
15–20 33.3 39.1 0.4941 a pregnant subject.
21–25 47.5 52.2
25–30 12.5 0.0
31–35 5.8 8.7 intervention and are often used in
35+ 0.8 0.0 clinical decision making regarding
Smoking prior to pregnancy further active periodontal therapy in
Yes 24.2 34.8 0.1877 patients undergoing initial periodon-
No 75.0 60.9 tal treatment (Table 3).
Smoking during pregnancy Preterm birth rates of <37 weeks
Yes 13.3 26.1 0.0825 GA for the 119 patients whose preg-
No 85.8 69.6 nancy outcomes could be determined
Alcohol/drug use
was 6.84%. Preterm birth rate
Yes 0.8 0.0 0.6634
No 98.3 95.7
<35 weeks GA in patients receiving
Total 119 23 intensive oral hygiene instructions
was 1.9% For the 87 patients who
*Marital status, education, smoking, alcohol variables missing on one enrolled patient. completed all oral hygiene visits, the
preterm birth rate <37 weeks GA
was 5.75% and for those patients
Table 2. Periodontal measurements at baseline and 8 weeks who were enrolled but did not com-
Mean (SD) Baseline 8 Weeks p-Value plete the study, the preterm birth
rate <37 weeks GA was 10.0%.
Plaque index 1.35 (1.28–1.43) 0.61 (0.54–0.69) <0.0001 These preterm birth rates did not
Gingival index 1.45 (1.38–1.51) 0.75 (0.68–0.81) <0.0001 differ significantly from historic con-
Probing depth 3.41 mm (3.31–3.52) 2.97 mm (2.87–3.07) <0.0001 trols recruited with the same inclu-
Clinical attachment levels 2.26 mm (2.16–2.37) 2.02 mm (1.92–2.12) <0.0001 sion/exclusion criteria approximately
10 years prior (Jeffcoat et al. 2001).

8 weeks post- intervention is illus-


Discussion
trated in Figs 1 and 2 respectively.
Mean number of baseline sites An increase in the clinical signs and
with PI ≥ 2 were 21.5 (SD = 14.4) symptoms associated with gingivitis
which was significantly reduced to without marked changes in the
10.1 (SD = 9.06) at 8 weeks after quantity of bacterial flora has been
prophylaxis and intensive oral noted in pregnant females (Maier &
hygiene measures. Similarly, the Orban 1949, L€ oe & Silness 1963, Co-
number of mean sites per individual hen et al. 1971, Kornman & Loesche
with GI ≥ 2 were significantly 1980, Tilakaratne et al. 2000, Taani
reduced from 30 sites (SD = 13.5) at et al. 2003, Figuero et al. 2013). The
baseline to 12 sites (SD = 11.3) at 8- levels of female gonadotropins dur-
week follow-up. The percentage of Fig. 1. Baseline frontal intraoral photo- ing pregnancy correlate with the
sites with PI ≥ 2 was 40% of sites graphs prior to intensive oral hygiene severity of gingivitis. Increased levels
(SD = 25) at baseline which regimen at 16 weeks gestation in a preg- of progesterone are associated with
decreased significantly to 17% of nant subject. increased membrane permeability,
sites (SD = 14.6) after prophylaxis which may contribute to vascular
and oral hygiene measures. GI ≥ 2 tion. These findings demonstrate an permeability and subsequent oedema
was present at 53% of sites overall decrease in detectable plaque of gingival tissues (O’Neil 1979,
(SD = 23) at baseline and 21.8% of and the signs and symptoms of gin- Raber-Durlcher et al. 1991, Raber-
sites (SD = 20.1) after the interven- gival inflammation after oral hygiene Durlacher et al. 1993). Furthermore,
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Hygiene regimen for pregnancy gingivitis 145

Table 3. Threshold Plaque index (PI) and Gingival index (GI) ≥ 2 at baseline and 8 weeks feedback and personalized care can
Baseline 8 weeks p-Value improve oral hygiene behaviours
(Niederman 2007, Renz et al. 2008).
PI ≥ 2 GI ≥ 2 PI ≥ 2 GI ≥ 2 Furthermore, younger patients have
been shown to benefit from repeated
Mean number 21.5 (14.4) 30.0 (13.5) 10.1 (9.06) 12.0 (11.3) <0.0001 sessions of prophylaxis and oral
of sites, n (SD) hygiene instructions (Hamp &
Mean percentage 40% (25) 53% (23) 17% (14.6) 21.8% (20.1) <0.0001 Johansson 1982), while all subjects
of sites, % (SD)
demonstrated overwhelmingly posi-
tive attitudes towards their oral
heath regardless of the current state
increasing salivary levels of estradiol Institute for Medicine 2007). As of their gingival condition (Bergen-
and progesterone have been corre- prevalence rates for pregnancy gingi- dal et al. 1982). This may indicate
lated with a 55-fold increase in the vitis have been reported between that, particularly for a young popu-
proportion of P. intermedia in the 36% and 100% (L€ oe & Silness 1963, lation, frequent personal interaction
bacterial flora during pregnancy L€oe 1965, Cohen et al. 1971, Jansen and emphasis on the significant
(Kornman & Loesche 1980, Jansen et al. 1981), an effective and non- health benefits of proper oral home
et al. 1981, Raber-Durlacher et al. invasive intervention to reduce gingi- care may be beneficial.
1994, Adriaens et al. 2009). This vitis could be a low cost, preventative The combined approach of one-
bacterial shift may be due to the measure to improve oral health in on-one oral hygiene counselling with
opportunistic substitution by P. in- primary care or public health set- a dentist or dental hygienist, DVD
termedia and other Bacteroides spp. tings. oral hygiene instruction, powered
of progesterone and oestrogen for The products included in the tooth brushing, dentifrice, dental
Vitamin K, and essential growth fac- home-care kit were selected based floss and cetylpyridinium chloride
tor (Kornman & Loesche 1982). Cochrane review data demonstrating mouth rinse, and dental prophylaxis
Oestrogen receptors (ERb) have improved oral hygiene outcomes in was effective in significantly reducing
been identified on gingival epithe- patients using an oscillating-rotating the whole-mouth PI, GI, PD and
lium and periodontal ligament mechanical toothbrush compared CAL values in pregnant patients
(J€
onsson et al. 2007, Nebel et al. with manual toothbrushes or other over an 8-week treatment time. Pre-
2011) and the direct effects of preg- powered or manual toothbrushes vious studies indicate that in the
nancy hormones on periodontal tis- (Robinson et al. 2005) and the absence of intervention, GI levels
sues (Mascarenhas et al. 2003) may adjunctive use of flossing as an effec- and/or bleeding upon probing (BOP)
account for an increase in gingivitis tive tool in the management of den- increased into the second trimester
incidence during pregnancy. tal caries and periodontal diseases in and remained elevated until parturi-
Despite the increased severity of adults (Sambunjak et al. 2011). Fur- tion (Adriaens et al. 2009, Buduneli
gingivitis and qualitative differences thermore, recent investigations have et al. 2010). Despite the elevated
in subgingival plaque composition in noted antimicrobial properties of hormone levels (Mealey & Moritz
pregnant females, in the absence of stannous fluoride dentifrice and the 2003) in these patients, the interven-
pathologic periodontal pocketing efficacy of 0.454% Stannous fluoride tion was effective in reducing the
and attachment loss, the condition is dentifrice in reducing gingival patients’ overall gingivitis levels. This
usually self-limiting and reversible inflammation as compared to posi- indicates that improved plaque
after parturition and/or lactation tive (tricolosan/copolymer) control removal is adequate to improve
when hormone balance is achieved. (He et al. 2012) and the effectiveness pregnancy gingiviitis. Many previous
Since gingivitis and its effects on the of cetyl pyridinium chloride mouthr- investigations did not consider pla-
periodontium are reversible there is inse in the reduction of preterm birth que levels when assessing clinical
a common misconception that a pro- rates in a high-risk population (Jeff- signs of gingival inflammation, it has
longed state of gingival inflammation coat et al. 2011a). been reported that plaque is the
during pregnancy does no potential Care was taken to evaluate study primary factor in GI findings during
harm. Because women with preg- participants at baseline and interme- pregnancy (Carrillo-De-Abornoz
nancy gingivitis demonstrate diate visits and assess their oral et al. 2012). While previous interven-
increased bleeding and gingival cre- hygiene to allow for individualized tions did include oral hygiene
vicular fluid production, the poten- interventions and most effectively instructions and/or monthly supra-
tial for bacteremias and increased eliminate clinical signs and symp- gingival tooth polishing (Mich-
serum levels of pro-inflammatory toms of gingival inflammation. Rep- alowicz et al. 2006), the regimen of
cytokines may make effective treat- etition and reinforcement of oral mechanical toothbrushing, floss,
ment of gingivitis during pregnancy hygiene instructions have been alcohol-free mouthrinse, a take-
important for overall maternal and shown to be critical in improving home instructional DVD discussing
foetal health. Reports identifying overall performance of oral hygiene oral hygiene and its importance, and
periodontal disease as a risk factor measures in periodontal patients monthly oral hygiene instructions
for preterm and low birth weight (Emler et al. 1980). Recent system- may have more effectively decreased
delivery underscore the need for atic reviews have demonstrated that pregnancy gingivitis. Further, since
improved oral care as a part of pre- application of psychological inter- the periodontal care was provided at
natal care (Offenbacher et al. 1996, ventions including individualized the Center for Women’s Reproductive
© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
146 Geisinger et al.

Health in conjunction with the sub- the efficacy of the proposed interven- of these interventions on pregnancy
jects’ prenatal visits, the connection tion as observed patients, particu- outcomes.
between periodontal and foetal/ larly pregnant women, may have
maternal health may have been a altered their hygiene habits strictly Conclusions
more impactful message leading to due to observation alone. While this
behavioural changes. Although some study design was based on previous An intensive regimen of repeated
subjects were lost to follow-up, the investigations that demonstrated and systematic oral hygiene instruc-
levels of non-compliance (19.3%) increasing gingivitis throughout tions combined with a multiproduct
with prenatal appointments in this pregnancy (L€ oe et al. 1965, Gursoy oral hygiene regimen was able to sta-
population are similar those demon- et al. 2008), future investigations tistically significantly reduce all clini-
strated in US populations with simi- should include a randomized con- cal signs of gingivitis in pregnant
lar demographics, which range from trolled trial study design with stan- women. This pilot study has resulted
23% to 44% (Haas et al. 1996, Riley dardized intervention procedures to in preliminary data on perinatal out-
et al. 2011). allow for additional conclusions comes that will allow sample size
A body of evidence exists that about the effectiveness about this calculation for a large-scale multi-
maternal periodontal disease and oral hygiene regimen in pregnant center controlled clinical trial.
oral inflammation are associated patients. Further investigation on
with preterm birth and low birth the effects of reducing gingivitis on
weight in infants (Jeffcoat et al. pregnancy outcomes is necessary and References
2001, Scannepieco et al. 2003, Wim- these data could allow for sample Adriaens, L. M., Alessandri, R., Sp€ orri, S., Lang,
mer & Pihlstrom 2008, Heimonen size calculations for large-scale con- N. P. & Persson, G. R. (2009) Does pregnancy
et al. 2009, Kunnen et al. 2010). trolled interventional studies on oral have an impact on the subgignival microbiota?
Journal of Periodontology 80, 72–81.
Despite these associations, large- and perinatal outcomes. Alzaharni, A. S., Bissada, N. F., Jurevic, R. J.,
scale interventional trials for peri- Furthermore, this intervention Naraendran, S., Nouneh, I. E. & Al-Zahrani,
odontal disease have been largely may be well suited for a widespread M. S. (2013) Reduced systemic inflammatory
ineffective (Michalowicz et al. 2006, public health intervention performed mediators after treatment of chronic gingivitis.
Saudi Medical Journal 34, 415–419.
Offenbacher et al. 2009, Ham 2010). by dental and/or medical auxiliary Arafat, A. H. (1974) Periodontal status during
This lack of effect may reflect a personnel. Rates of pregnancy gingi- pregnancy. Journal of Periodontology 45, 641–
focus on treating periodontal disease vitis have been demonstrated to be 643.
and periodontal clinical attachment higher in African American women Bergendal, B., Erasmie, T. & Hamp, S. E. (1982)
Dental prophylaxis for youths in their late
loss without a concomitant focus on (Lieff et al. 2004) and those with teens. III. Attitudes to teeth and dental health
the elimination of gingivitis. lower socio-economic status (Sarlati and their relation to dental health behavior.
Periodontal disease severity has et al. 2004). In these high-risk popu- Journal of Clinical Periodontology 9, 46–56.
been linked to the same pro-inflam- lations, low cost interventions may Buduneli, N., Becerik, S., Buduneli, E., Baylas,
H. & Kinnby, B. (2010) Gingival status, crevic-
matory markers, such as C-reactive result in overall improvement of
ular fluid tissue-type plasminogen activator
protein (CRP), IL-1, IL-6, tumour maternal and foetal oral and sys- inhibitor-2 levels in pregnancy versus post-
necrosis factor alpha (TNF-a), plate- temic health. Limitations for large- partum. Australian Dental Journal 55, 292–297.
let-derived growth factor (PDGF) scale application of this type of Carrillo-De-Abornoz, A., Figuero, E., Herrera,
and transforming growth factor-beta treatment may include, cost–benefit D., Cuesta, P. & Bascones-Martinez, A. (2012)
Gingival changes during pregnancy III. Implact
(TGF-b) that are associated with analysis of the cost of the study of clinical, microbiological, immunological, and
preterm births (Kornman et al. 1997, materials and personnel require- sociodemographic factors on gingival inflam-
Reddy et al. 2003, Lyttle et al. 2009, ments as compared with the eco- mation. Journal of Clinical Periodontology 39,
Eberhard et al. 2013). Furthermore, nomic and health benefits of the 272–283.
Chambrone, L., Guglielmetti, M. R., Pannuti, C.
periodontal intervention has been intervention on oral health and preg- M. & Chambrone, L. A. (2011a) Evidence
shown to decrease serum levels of nancy outcomes. Further studies grade associating periodontitis to preterm birth
these markers, with the greatest may focus on the feasibility and and/or low birth weight: I. A systematic review
reduction seen in patients who dem- cost-utility analysis (CUA; Cohen of prospective cohort studies. Journal of Clini-
cal Periodontology 38, 795–808.
onstrated decreases in clinical mea- 2003) of application of these inter- Chambrone, L., Guglielmetti, M. R., Pannuti, C.
sures of gingival inflammation ventions for public health and in M. & Chambrone, L. A. (2011b) Evidence
(D’Aiuto et al. 2004, Alzaharni et al. clinical practice. grade associating periodontitis to preterm birth
2013). This pilot study may have This study included the preg- and/or low birth weight: II. A systematic
review of randomized controlled trials evaluat-
identified a novel approach for inter- nancy outcome data so that other
ing the effects of periodontal treatment. Journal
vention in pregnant patients with research groups could use the data of Clinical Periodontology 38, 902–914.
pregnancy gingivitis. for planning the treatment timing Cohen, B. J. (2003) Discounting in cost-utility
A disadvantage of this study and intensity of randomized control analysis of healthcare interventions: reassessing
design is the lack of control subjects trials. Care should be taken not to current practice. Pharmacoeconomics 23, 75–87.
Cohen, D. W., Shapiro, J., Friedman, L., Kyle,
who were observed, but did not interpret the data as an indication G. C. & Franklin, S. (1971) A longitudinal
receive prophylaxis and intensive that eliminating gingivitis with an investigation of the periodontal changes during
oral hygiene instructions during oral hygiene regimen reduces the pregnancy and fifteen months post-partum. II.
pregnancy. This approach, while it incidence of preterm birth in preg- Journal of Periodontology 42, 653–657.
D’Aiuto, F., Ready, D. & Tonetti, M. S. (2004)
allows for observations and pilot nant women. Additional larger scale Periodontal disease and C-reactive protein
data for future trials, does not allow prospective interventional trials are associated cardiovascular risk. Journal of Peri-
for conclusions to be made regarding needed to determine the true effect odontal Research 39, 236–241.

© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Hygiene regimen for pregnancy gingivitis 147

Eberhard, J., Grote, K., Luchtefeld, M., Heuer, Nilsson, B. O. (2007) Demonstration of mit- Mitchell, D. A., Matseonane, S. & Tschida, P.
W., Schuett, H., Divchey, D., Scherer, R., Sch- ochrondrial oestrogen receptor beta and oestro- A.; OPT Study (2006) Treatment of periodon-
mitz-Streit, R., Langfeldt, D., Stumpp, N., gen-induced attenuation of cytochrome c tal disease and the risk of preterm birth. New
Staufenbiel, I., Schieffer, B. & Stiesch, M. oxidase subunit I expression in human peri- England Journal of Medicine 355, 1885–1894.
(2013) Experimental gingivitis induces systemic odontal ligament cells. Archives of Oral Biology Nebel, D., Bratthall, G., Ekblad, E., Norderyd,
inflammatory markers in young healthy indivi- 52, 669–676. O. & Nilsson, B. O. (2011) Estrogen regulates
duals: a single-subject interventional study. Kinny, B., Matsson, L. & Astedt, B. (1996) DNA synthesis in human gingival epithelial
PLoS ONE 8, e55265. Aggravation of gingival inflammatory symp- cells displaying strong estrogen receptor b
Emler, B. F., Windchy, A. M., Zaino, S. W., toms during pregnancy associated with the con- immunoreactivity. Journal of Periodontal
Feldman, S. M. & Scheetz, J. P. (1980) The centration of plasminogen activator inhibitor Research 46, 622–628.
value of repetition and reinforcement in type 2 (PAI-2) in gingival fluid. Journal of Peri- Ness, P. M. & Perkins, H. A. (1980) Transient
improving oral hygiene performance. Journal of odontal Research 31, 271–277. bacteremia after dental procedures and minor
Periodontology 51, 228–234. Kornman, K. S. & Loesche, W. J. (1980) The manipulations. Transfusion 20, 82–85.
Figuero, E., Carillo-de-Albornoz, A., Herrera, D. subgingival microflora during pregnancy. Jour- Niederman, R. (2007) Psychological approaches
& Bascones-Martınez, A. (2010) Gingival nal of Periodontal Research 15, 111–122. may improve oral hygiene behaviour. Evidence-
changes during pregnancy: I. Influence of hor- Kornman, K. S. & Loesche, W. J. (1982) Effects of Based Dentistry 8, 39–40.
monal variations on clinical and immunological estradiol and progesterone on Bacteroides mel- Offenbacher, S., Beck, J. D., Jared, J. L., Mauri-
parameters. Journal of Clinical Periodontology aningenicus. Infection and Immunity 35, 256–263. ello, S. M., Mendoza, L. C., Couper, D. J.,
37, 220–229. Kornman, K. S., Page, R. C. & Tonetti, M. S. Stewart, D. D., Murtha, A. P., Cochran, D. L.,
Figuero, E., Carrillo-de-Albornoz, A., Martın, C., (1997) The host response to the microbial chal- Dudley, D. J., Reddy, M. S., Geurs, N. C. &
Tobıas, A. & Herrera, D. (2013) Effect of preg- lenge in periodontitis: assembling the Players. Hauth, J. C.; for the Maternal Oral Therapy to
nancy on gingival inflammation in systemically Periodontology 2000 13, 33–53. Reduce Obstetric Risk (MOTOR) Investigators
healthy women: a systematic review. Journal of Kunnen, A., van Doormaal, J. J., Abbas, F., Aar- (2009) Effects of peridontal therapy on rate of
Clinical Periodontology 40, 457–473. noudse, J. G., van Pampus, M. G. & Faas, M. preterm delivery. A randomized controlled
Gursoy, M., Pajukanta, R., Sorsa, T. & Kononen, M. (2010) Periodontal disease and pre-eclamp- trial. Obstetrics and Gynecology 114, 551–559.
E. (2008) Clinical changes in periodontium dur- sia: a systematic review. Journal of Clinical Offenbacher, S., Katz, V., Fertik, G., Collins, J.,
ing pregnancy and post-partum. Journal of Periodontology 37, 1075–1087. Boyd, D., Maynor, G., McKaig, R. & Beck, J.
Clinical Periodontology 35, 576–583. Lieff, S., Boggess, K. A., Murtha, A. P., Jared, (1996) Periodontal disease as a possible risk
Haas, J. S., Berman, S., Goldberg, A. B., Lee, L. H., Madianos, P. N., Moss, K., Beck, J. & Of- factor for preterm low birth weight. Journal of
W. K. & Cook, E. F. (1996) Prenatal hospital- fenbacher, S. (2004) The oral conditions and Periodontology 67 (Suppl), 1103–1113.
ization and compliance with guidelines for pre- pregnancy study: periodontal status of a cohort Offenbacher, S., Lieff, S., Bogess, K. A., Murtha,
natal care. American Journal of Public Health of pregnant women. Journal of Periodontology A. P., Madianos, P. N., Champagne, C. M.,
86, 815–819. 75, 116–125. McKaig, R. G., Jared, H. L., Mauriello, S. M.,
Ham, Y. W. (2010) Oral health and adverse preg- L€
oe, H. (1965) Periodontal changes in pregnancy. Auten, R. L. Jr, Herbert, W. N. & Beck, J. D.
nancy outcomes – what’s next? Journal of Den- Journal of Periodontology 36, 209–216. (2001) Maternal periodontitis and prematurity.
tal Research 90, 289–293. L€
oe, H. (1967) The gingival index, the plaque Part I: obstetric outcome of prematurity and
Hamp, S. E. & Johansson, L. A. (1982) Dental index and the retention index systems. Journal growth restriction. Annals of Periodontology 6,
prophylaxis for youths in their late teens. I. of Periodontology 38 (Suppl), 610–616. 164–174.
Clinical effect of different preventative regimes L€
oe, H. & Silness, J. (1963) Periodontal disease in O’Neil, T. C. A. (1979) Plasma female sex hor-
on oral hygiene, gingivitis, and dental caries. pregnancy I. Prevalence and severity. Acta Od- mone levels and gingivitis in pregnancy. Journal
Journal of Clinical Periodontology 9, 22–34. ontologica Scandinavica 21, 533–551. of Periodontology 50, 279–282.
He, T., Barker, M. L., Biesbrock, A. R., Sharma, L€
oe, H., Theilade, E. & Jensen, S. B. (1965) Raber-Durlacher, J. E., Leen, W., Palmer-Bouva,
N. C., Qaqish, J. & Goyal, C. R. (2012) Experimental gingivitis in man. Journal of Peri- C. C., Raber, J. & Abraham-Inpijn, L. (1993)
Assessment of the effects of a stannous fluoride odontology 36, 177. Experimental gingivitis during pregnancy and
dentifrice on gingivitis in a two-month positive- Lopatin, D. E., Kornman, K. S. & Loesche, W. J. post-partum: immunohistochemical aspects.
controlled clinical study. The Journal of Clinical (1980) Modulation of immunoreactivity to peri- Journal of Periodontology 50, 211–218.
Dentistry 23, 80–85. odontal disease-associated microorganisms during Raber-Durlacher, J. E., Van Steenbergen, T. J.,
Heimonen, A., Janket, S. J., Kaaja, R., Ackerson, pregnancy. Infection and Immunity 28, 713–718. Van Der Velden, U., De Graaff, J. & Abra-
L. K., Muthukrishnan, P. & Meurman, J. H. Lopez, N. J., DaSilva, I., Ipinza, J. & Gutierrez, ham-Inpijn, L. (1994) Experimental gingivitis
(2009) Oral Inflammatory Burden and Preterm J. (2005) Periodontal therapy reduces the rate during pregnancy and post-partum: clinical,
Birth. Journal of Periodontology 80, 884–891. of preterm low birth weight in women with endocrinological, and microbiological aspects.
Institute for Medicine (2007) Preterm Birth: Causes, pregnancy-associated gingivitis. Journal of Peri- Journal of Clinical Periodontology 21, 549–
Consequences, and Prevention. Washington, DC: odontology 76, 2144–2153. 558.
National Academy Press. URL: www.marchofdi- Lyttle, B., Chai, J., Gonzalez, J. M., Xu, H., Raber-Durlcher, J. E., Zeijlemaker, W. P., Me-
mes.com/peristats/ (accessed 11 November 2013). Sammel, M. & Elovitz, M. A. (2009) The nega- inesz, A. A. & Abraham-Inpijn, L. (1991) CD4
Jansen, J., Liljermark, W. & Bloomquist, C. tive regulators of the host immune response: an to CD8 ratio and in vitro lymphoproliferative
(1981) The effect of female sex hormones on unexplored pathway in preterm birth. American responses during experimental gingivitis in
subgingival plaque. Journal of Periodontology Journal of Obstetrics and Gynecology 201, pregnancy and post-partum. Journal of Peri-
52, 599–602. 284.e1–284.e7. odontology 62, 663–667.
Jeffcoat, M. K., Geurs, N. C., Reddy, M. S., Maier, A. W. & Orban, B. (1949) Gingivitis in Reddy, M. S., Geurs, N. C. & Gunsolley, J. C.
Cliver, S. P., Goldenberh, R. L. & Hauth, J. C. pregnancy. Oral Surgery Oral Medicine Oral (2003) Periodontal host modulation with anti-
(2001) Periodontal infection and preterm birth: Pathology 2, 334–373. proteinase, anti-inflammatory, and bone spar-
results of a prospective study. Journal of the Mariotti, A. (1994) Sex steroid hormones and cell ing agents: a systematic review. Annals of
American Dental Association 132, 875–880. dynamics in the periodontium. Critical Reviews Periodontology 8, 12–37.
Jeffcoat, M., Parry, S., Gerlach, R. W. & Doyle, in Oral Biology and Medicine 5, 27–53. Renz, A., Ide, M., Newton, T., Robinson, P. G.
M. J. (2011a) Use of alcohol-free antimicrobial Mascarenhas, P., Gapski, R., Al-Shammari, K. & & Smith, D. (2008) Psychological interventions
mouthrinse is associated with decreased inci- Wang, H. L. (2003) Influence of sex hormones to improve adherence to oral hygiene instruc-
dence of preterm birth in a high-risk popula- on the periodontium. Journal of Clinical Peri- tions in adults with periodontal diseases. (2007)
tion. American Journal of Obstetrics and odontology 30, 671–678. Cochrane Database Systematic Review Issue 4,
Gynecology 205, 382e1–382e6. Mealey, B. L. & Moritz, A. J. (2003) Hormonal Art No: CD005097.
Jeffcoat, M., Parry, S., Sammel, M., Clothier, B., influences: effects of diabetes mellitus and Riley, M., Galang, S. & Green, L. A. (2011) The
Caitlin, A. & Macones, G. (2011b) Periodontal endogenous female sex steroid hormones on impact of clinical reminders on Prenatal care.
infection and preterm birth: successful peri- the periodontium. Periodontology 2000 32, 59– Family Medicine 43, 560–565.
odontal therapy reduces the risk of preterm 81. Robinson, P. G., Deacon, S. A., Deery, C., Hea-
birth. BJOG 118, 250–256. Michalowicz, B. S., Hodges, J. S., DiAngelis, A. nue, M., Walmsley, A. D., Worthington, H. V.,
J€
onsson, D., Nilsson, J., Odenlund, M., Bratthall, J., Lupo, V. R., Novak, M. J., Ferguson, J. E., Glenny, A. M. & Shaw, W. C. (2005) Manual
G., Broman, J., Ekblad, E., Lydrup, M. L. & Buchanan, W., Bofill, J., Papapanou, P. N., versus powered toothbrushing for oral health.

© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
148 Geisinger et al.

Cochrane Database Systematic Review Issue 2, Scannepieco, F. A., Bush, R. B. & Paju, S. (2003) intracrevicular prostaglandin E2 concentrations
Art. No.: CD002281. Periodontal disease as a risk factor for adverse and clinical parameters in pregnancy. Journal
Rode Sde, M., Gimenez, X., Montoya, V. C., Go- pregnancy outcomes. A systematic review. of Periodontology 73, 173–177.
mez, M., Blanc, S. L., Medina, M., Salinas, E., Annals of Periodontology 8, 70–78. Zaki, K., El Hak, R., Amer, W., Saleh, F., El
Pedroza, J., Zaldivar-Chiapa, R. M., Pannuti, Taani, D. Q., Habashneh, R., Hammad, M. M. & Faras, A., Ragab, L. & Nour, H. (1984) Sali-
C. M., Cortelli, J. R. & Oppermann, R. V. Batieha, A. (2003) The periodontal status of vary female sex hormone levels and gingivitis
(2012) Daily biofilm control and oral health: pregnant women and its relationship with in pregnancy. Biomedica Biochimica Acta 43,
consensus on the epidemiological challenge— socio-demongraphic and clinical variables. 749–754.
Latin American Advisory Panel. Brazilian Oral Journal of Oral Rehabilitation 30, 440–445.
Research 26(Suppl), 133–143. Tilakaratne, A., Soory, M., Ranasinghe, A. W.,
Sambunjak, D., Nickerson, J. W., Poklepovic, T., Corea, S. M., Ekanayake, S. L. & Silva, M. Address:
Johnson, T. M., Imai, P., Tugwell, P. & Wor- (2000) Periodontal disease status during preg- Maria L. Geisinger, DDS
thington, H. V. (2011) Flossing for the man- nancy and 3 months post-partum, in a rural Department of Periodontology
agement of periodontal diseases and dental population of Sri Lankan women. Journal of School of Dentistry
caries in adults (Review). Cochrane Database Clinical Periodontology 27, 787–792. University of Alabama at Birmingham
Systematic Review Issue 12, Art. No: Wimmer, G. & Pihlstrom, B. L. (2008) A critical SDB 412
CD008829. assessment of adverse pregnancy outcome and
Sarlati, F., Akhondi, N. & Jahanbakhsh, N. periodontal disease. Journal of Clinical Peri-
1720 2nd Avenue South
(2004) Effect of general health and sociocul- odontology 35 (Suppl), 380–397. Birmingham, AL 35294-007
tural variables on periodontal status of preg- Yalcin, F., Basegmez, C., Isik, G., Berber, L., Es- USA
nant women. Journal of the International kinazi, E., Soydine, M., Issever, H. & Onan, E-mail: miagdds@uab.edu
Academy of Periodontology 6, 95–100. U. (2002) The effects of periodontal therapy on

gingival inflammation and pregnancy treatment of gingivitis in pregnant


Clinical Relevance
outcomes. women reduces preterm birth rates.
Scientific rationale for the study: To Principal findings: An intense oral Practical implications: Treating gin-
evaluate a protocol to reduce or hygiene regimen reduces clinical givitis in pregnant women is critical
prevent the progression of gingivi- measures of gingivitis in pregnant to improving their oral health. An
tis during pregnancy and provide women. This study provides pilot intensive oral hygiene regimen is a
pilot data for future randomized data for planning the timing and minimally invasive, cost-effective
controlled trials evaluating inter- intensity of further randomized con- method of treating gingivitis in
ventions in pregnant women on trolled clinical trials to determine if pregnant patients.

© 2013 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

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