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nvw;) JOURNAL OF CLINICAL MEDICINE OF KAZAKHSTAN ..... Original Article
(E-ISSN 2313-1519)
The impact of periodontitis on the risk of preterm birth: Systematic review and meta-analysis
Zhibek Oralkhan1, Gurpreet Singh Walia2, Gulmira Zhurabekova1, Akzhenis Berdalinovau, Ibrahim Abdelazim4, Erasyl Kabi5, Lazzat Bimaganbetova6
'Al-Farabi Kazakh National University, Almaty, Kazakhstan
2S.D. Asfendiyarov Kazakh National Medical University, Almaty, Kazakhstan
West Kazakhstan Marat Ospanov State Medical University, Aktobe, Kazakhstan
4Ain Shams University, Cairo, Egypt
5Atyrau Regional Perinatal Center, Atyrau, Kazakhstan
6Kyzylorda Regional Perinatal Center, Kyzylorda, Kazakhstan
Abstract
Background: Preterm birth (PTB) is one of the most prevalent and serious adverse pregnancy outcomes (APOs) and major health risk for pregnant individuals and their children during pregnancy and throughout their lifespan. Periodontitis has long been regarded as a silent pandemic which happens to favor the pregnant women due to the physical and hormonal changes during pregnancy. Understanding of the association underscores the importance of keeping oral diseases under check and control to predict and even reduce the risk. The aim is to evaluate the association between periodontitis during pregnancy and preterm birth.
Material and methods: A screening and analysis was conducted on studies with comparison data about periodontal infection diseases during pregnancy and preterm birth. The databases include Scopus, PubMed, Elibrary, local databases and the Cochrane library and were searched up to November 20, 2022. The selected studies were included in a random-effects meta-analysis after evaluation of the methodological quality. The summary odds ratios (ORs) with 95% confidence intervals (CI) were calculated with Review Manager software.
Results: The review finally included 29 studies involving 2606589 pregnant women. Compared with healthy oral status in pregnancy, periodontitis was associated with preterm birth [OR=1.81, CI=1.60 to 2.03; p<0.001; I2 = 95%].
Conclusion: Periodontitis as one of the important factors is associated with increased risks of preterm birth. It is important to put the disease under control before and during pregnancy to reduce the preterm birth outcome.
Key words: pregnancy, preterm birth (PTB), periodontitis
Received: 2023-03-11. Accepted: 2023-04-24
© ®
This work is licensed under a Creative Commons Attribution 4.0 International License
J Clin Med Kaz 2023; 20(3):56-62
Corresponding author: Zhibek Oralkhan. E-mail: [email protected];
Introduction
Preterm birth is a serious medical condition and remains one of the most intransigent research problems in obstetrics and gynecology in the world. According to the statistics, there were 1 in 10 babies born preterm, of these, 80% were born in Asia and Africa [1]. In Kazakhstan, this figure was 8.8 % and increased to 15.2% in 2017 [2]. According to experts of the Statistics Committee of the Ministry of National Economy in the country, despite the
fact that the overall infant mortality rate in the country has decreased, these figures are still disappointing. In the Atyrau, Almaty and Aktobe regions, infant mortality is still high. In one center of the country alone, about 350 children are treated annually. About 200 of them were born prematurely.
The sequelae of preterm birth for the children ranging from significant morbidity such as mental retardation, vision impairment and cerebral palsy, to
mortality of the offsprings [3]. In the long term, preterm birth increased risk for cardiovascular disease, diabetes and cancer as an adult [3,4]. For the mother, delivering preterm increases her risk of a subsequent preterm delivery [4].
To date, advances in maternal prenatal care, increased public awareness and progress has been made in identifying the factors that may be connected with prematurity, as well as ruling out certain treatments that have not been shown to be effective
[5]. Infection and host inflammatory response has long been associated with adverse pregnancy outcomes, including PTB
[6]. Periodontitis has long been regarded as a silent pandemic which happens to favor pregnant women due to the physical and hormonal changes. It reported that periodontitis occurs about 2 to 3 times more often than genitourinary tract infections [7]. The role of periodontitis as one of the causation of adverse pregnancy outcomes such as pre-eclampsia, gestational diabetes, preterm delivery, low birth weight infants has been extensively evaluated from observational evidence [8]. Periodontitis is a preventable and treatable disease, and it is thus necessary to identify the most common and representative predisposing factors among pregnant women may have a contribution to update a prenatal and perinatal oral health care protocol. Thus a better understanding of the nature of this association will assist in treatment planning to reduce adverse pregnancy outcomes.
This review considers whether the maternal periodontitis as a potential risk factor for preterm birth while there have been more and more recent studies reported conflicting results.
Material and methods
The study was conducted according to PRISMA guidelines [9]. The research question was generated as whether there was a higher risk of preterm birth among periodontitis affected pregnant population compared to the one with healthy periodontium. The databases include Scopus, PubMed, Elibrary, local databases and the Cochrane library and were searched up to November 20, 2022. Medical Subject Headings (MeSH) terms and keywords set as "Periodontal disease OR Periodontitis" AND "pregnancy". Two authors screened the titles and abstracts after searching the databases and involved studies for final evaluation. All of the full text available articles evaluating oral health status during pregnancy and maternal and infant outcomes that met the following inclusion criteria were scrutinized and selected: observational study; population included pregnant people; Oral health status were evaluated with periodontal examination; comparisons included pregnant women with periodontitis versus those without periodontitis or with controlled status; outcomes included preterm birth. Reviews, Meta analyses, case reports, case series and abstracts were excluded from the study.
The following data was extracted from the studies included: author with year of publication, design of the study, the number of participants included in the study, definition of the oral diseases including periodontitis. The characteristics of the included studies are described in Table 1. Newcastle-Ottawa Scale was used to assess quality of the studies (Table 2).
Statistical analysis
Review Manager 5.4 was used to analyze the data extracted from the included studies. The associations between oral diseases and preterm birth and low birth weight were assessed and measures of effect were presented as odds ratios (ORs) with 95% confidence intervals (CIs). The heterogeneity between studies was assessed with I2 statistics. The analysis was considered significant when P<0.05.
Results
The search strategy resulted in 1487 potentially relevant citations. 1304 initially searched studies excluded from further analysis after screening the title and abstract. The PRISMA Flow Diagram (Figure 1) summarizes the process of literature search and selection of studies. After screening the titles and abstracts, we read 67 full-text papers and included 29 studies with comparable outcomes [10-38].
Among the 2606589 pregnant participants, 827223 of them with maternal periodontitis and 1779366 unaffected pregnant controls assessed the oral infection on preterm birth in this study, compared with pregnant women without periodontitis, the pregnant women with periodontitis regardless of the diagnostic criteria and other factors were at higher risk of experience preterm birth [OR =1.81, CI = 1.60 to 2.03; p<0.001; I2=95%] (Figure 2). A funnel plot was plotted and egger's test was conducted to assess the presence of potential publication bias (Figure 3). There was no potential publication bias found (Table 3).
Discussion
Periodontal disease and other oral health problems have been supposed to be a risk factor for preterm birth in many literatures [2,8]. This systematic review and meta-analysis focuses on the most common and severe oral disease namely periodontitis with one of the adverse pregnancy outcomes, preterm birth. Our result found maternal periodontitis during pregnancy is associated with preterm birth compared with periodontal healthy pregnancies. This finding suggests that the health care system should adopt effective strategies to keep oral diseases under check and control to predict and even reduce the risk of exhibiting pregnancy related adverse outcomes.
Although several previous systematic review and meta-analysis regards the periodontitis and adverse pregnancy outcomes reported positive correlation between periodontitis and preterm birth [8], all of the studies showed the need for updating evidence while the number of well-designed publications from observational to experimental studies on this topic have been increased along with time.
The present study was based on the last global and local data, with more observed outcomes. As our results, the 29 individual studies included in the present investigation, which can be considered conflicting, since several of them indicate that there is no association between two health conditions. Another findings of our data searching and screening the methodological quality and design of the original data showed that local or neighbor studies from Central Asia on the aspect of oral health and its relation to maternal and child health is scarce. Well-designed evidence with clear diagnostic criteria of diseases with consideration of confounding factors are needed for contributing to the international database, while regional, genetic, dietary, hygiene, and health care differences contribute to different risks.
In accordance with the previously published systematic reviews, Our meta-analysis also suggests that the periodontitis during the pregnancy is one of the risk factors for occurrence of the preterm birth while the disease is multifactorial in nature. The mechanisms underlying the association could be explained by the theory that set as the periodontal pathogens may trigger an inflammatory response leading to elevated inflammatory cytokines level which would influence the degradation of the extracellular matrix of the fetal membranes and cervix [6,7]. It also could be explained as the periodontal pathogens, such as Fusobacterium nucleatum, migrates to the fetal-placental
Table 1
Characteristics of the included studies
Study Country Design Blind Participants Age Examination PD definition Conclusion
Control/case
2022 Iqbal A India Retrospective NA 4/100,7/100 23-24 Before delivery NA No association , p=0.189
2022 Pockpa ZAD Ivory Coast Prospective Yes 12/137,50/201 15-50 Before delivery 2018 EFP/AAP Positive association,OR = 3.62
2022 Lee YL Taiwan Retrospective Yes 97447/ 825399,93589/ 728643 20-45 Before delivery AAP OR=1.09
2022 Trivedi P India Prospective Yes 143/1897,37/ 80 24.6 Before delivery Irritation, redness, and swelling of the gums. OR= 11.4
2022 Shaggag LM Sudan Case-control Yes 115/250,50/ 80 22-36 After delivery EFP/AAP OR=2.05
2021 Choi SE USA Retrospective Yes 105346 / 731081,2935/ 15979 27.8/31.6 Before delivery Treatment pre pregnancy OR=1.15
2021 Márquez-Corona ML Mexico Case-control NA 6/32,10/79 18-42 Before delivery CDC-AAP Positive
2021 Uwambaye P Rwanda Case-control Yes 31/260,154/ 295 16-35 After 1 to 5days Delivery EFP/AAP OR=6.36
2020 Micu IC Romania Case-control Yes 54/156,20/38 18-43 within the first 72 h after delivery AAP OR=2.18
2020 Nikolic L Serbia Cross sectional NA 19/68,37/44 17-41 within 48 hours following delivery 1999 Positive
2020 Moncunill-Mira J Spain Case-control Yes 28/82,32/64 18-45 the first 2 days of the postpartum AAP OR= 7.49
2020 Novák T Hungary Case-control Yes 44/165,33/77 29.3/ 3 days post-par- tum. PD >4 mm found at least at one site, and BOP >50% of the teeth. OR=1.95
2020 de Oliveira LJC Brazil Prospective Yes 299/ 2239,39/362 20-34 Before delivery AAP OR=1.93
2020 Erchick DJ Nepal Prospective Yes 113/ 840,84/554 15-40 Before delivery BOP >10% and/or PD >4 mm OR=1.07
2020 Taniguchi-Tabata A Japan Prospective Yes 1/21,4/23 34.1 first or early second trimester. EM Positive
2019 Pérez-Molina JJ Mexico Case-control NA 114/522,229/ 507 23.8 /23.2 first 24 hours of the NB delivery EM CDC-AAP OR 2.95
2019 Kopycka-Kedzierawski DT USA Retrospective NA 18292/ 211966,6231/ 77247 27.7/27.3 After delivery Bleeding swollen gum OR=0.950 No association
2018 Lafaurie GI Colombia Case control NA 51/296,22/69 NA After delivery CPI index OR=2.04
2018 Gesase N Tanzania Cross sectional 79/958,31/ 159 18-46 the time of admission to the labour and delivery area CPI index OR=2.7
2018 Montenegro DA Colombia Case control NA 30/91,52/105 24,24.1 before or up to 8 hours after the delivery AAP OR=1.99
2017 Govindasamy R India Cross sectional NA 653/1556,747/ 1944 18-35 within 3 days of delivery AAP OR=0.72
2016 Khan NS Pakistan Case Control NA 31/89,49/71 18-35 within the first 48 hours EM OR =3.173
2015 Blanc V Spain Case Control Yes 18/29,18/28 24 24 h from delivery EM No
2015 Basha S India Prospective NA 17/181,20/126 18-28 After delivery EM OR= 4.54
2014 Macedo JF Brazil Case-control NA 58/250,16/46 42/222,32/74 18-40 within the first 48 h after delivery EM OR=1.98
2013 Ashok Kumar India Prospective 24/132,23/61 20-35 at 14-20 weeks CPI index OR=2.72
2013 Wang YL Taiwan RCT Yes 11/149,11/62 22-40 <5 months gestation AAP No
2013 Santa Cruz Spain Prospective NA 3/116,2/54 NA Before delivery EFP No
2012 Tejada Switzerland Case-control Yes 50/304,34/125 NA cwithin 24-72 h following delivery AAP Positive
NA means not available.
CAL clinical attachment loss, PD probing depth
CDC-AAP: absent: PD<3mm and CAL<2mm; mild: PD>3mm or CAL>2mm; moderate: two or more sites with PD > 5mm and two or more sites with
CAL>2mm; and severe: four or more sites with PD>5 mm and four or more sites with CAL>2 mm.
EFP/AAP classification, interdental CAL at two non-adjacent teeth with buccal/oral CAL>3 mm, with pocketing >3 mm
CPI index: Clinical attachment loss and probing depth mm in one or more site
EM: least four teeth with one or more sites with a probing depth of >4 mm and with clinical attachment loss of >3 mm [41]
Table 2
Assessment of quality of the included studies using Newcastle-Ottawa Scale.
Study Selection Comparability Exposure/ outcome Total
2022 Iqbal A *** * ** 6
2022 Pockpa ZAD *** ** *** 8
2022 Lee YL *** ** *** 8
2022 Trivedi P ** ** ** 6
2022 Shaggag LM *** ** ** 7
2021Choi SE *** ** *** 8
2021 Márquez-Corona ML ** * ** 5
2021 Uwambaye P *** * ** 6
2020 Micu IC *** ** ** 7
2020 Nikolic L ** * *** 6
2020 Moncunill-Mira J *** ** ** 7
2020 Novák T *** * *** 7
2020 de Oliveira LJC *** ** *** 8
2020 Erchick DJ *** * ** 6
2020 Taniguchi-Tabata A * ** ** 5
2019 Pérez-Molina JJ *** ** ** 7
2019 Kopycka-Kedzierawski DT **** ** ** 8
2018 Lafaurie GI *** * ** 6
2018 Gesase N *** * ** 6
2018 Montenegro DA *** ** ** 7
2017 Govindasamy R *** * ** 6
2016 Khan NS *** * ** 6
2015 Blanc V ** ** ** 6
2015 Basha S *** * ** 6
2014 Macedo JF ** ** ** 6
2013 Ashok Kumar *** ** *** 8
2013 Wang YL **** ** *** 9
2013 Santa Cruz *** * ** 6
2012 Tejada ** ** ** 6
Periodontitis
Healthy
Odds Ratio
Study or Subgroup Events Total Events Total Weight M-H, Random, 95% CI Year
Tejada 2012 34 125 50 304 3.5% 1.90 [1.15, 3.12] 2012
Ashok Kumar 2013 23 61 24 132 2.3% 2.72 [1.38, 5.38] 2013
Santa Cruz 12013 2 54 3 116 0.4% 1.45 [0.23, 8.93] 2013
Wang YL 2013 11 62 11 149 1.5% 2.71 [1.11, 6.62] 2013
Macedo JF 2014 16 46 58 250 2.3% 1.77 [0.90, 3.46] 2014
Basha S 2015 20 126 17 181 2.2% 1.82 [0.91, 3.63] 2015
Blanc V 2015 18 28 18 29 1.1% 1.10 [0.37, 3.23] 2015
Khan NS 2016 49 71 31 89 2.3% 4.17 [2.14, 8.11] 2016
Govindasamy R 2017 747 1944 653 1556 7.9% 0.86 [0.75, 0.99] 2017
Gesase N 2018 31 159 79 958 3.9% 2.69 [1.71, 4.25] 2018
Lafaurie GI 2018 22 69 51 296 2.8% 2.25 [1.25, 4.05] 2018
Montenegro DA 2018 52 105 30 91 2.8% 1.99 [1.12, 3.57] 2018
Kopycka-Kedzierawski DT 2019 6231 77247 18292 211966 8.8% 0.93 [0.90, 0.96] 2019
Pérez-Molina JJ 2019 229 507 114 522 6.1% 2.95 [2.25, 3.87] 2019
de Oliveira LJC 2020 39 362 299 2239 5.0% 0.78 [0.55, 1.12] 2020
Erchick DJ 2020 84 554 113 840 5.6% 1.15 [0.85, 1.56] 2020
Micu IC 2020 20 38 54 156 2.1% 2.10 [1.02, 4.30] 2020
Moncunill-Mira J 2020 32 64 28 82 2.3% 1.93 [0.99, 3.77] 2020
Nikolic L 2020 37 44 19 68 1.3% 13.63 [5.19, 35.82] 2020
Novák T 2020 33 77 44 165 2.9% 2.06 [1.17, 3.64] 2020
Taniguchi-Tabata A 2020 4 23 1 21 0.3% 4.21 [0.43, 41.14] 2020
Choi SE 2021 2935 15979 105346 731081 8.7% 1.34 [1.28, 1.39] 2021
Márquez-Corona ML 2021 10 79 6 32 1.0% 0.63 [0.21, 1.90] 2021
Uwambaye P 2021 154 295 31 260 4.0% 8.07 [5.20, 12.52] 2021
Iqbal A 2022 7 100 4 100 0.8% 1.81 [0.51, 6.38] 2022
Lee YL 2022 93589 728643 97447 825399 8.8% 1.10 [1.09, 1.11] 2022
Pockpa ZAD 2022 50 201 12 137 2.3% 3.45 [1.76, 6.76] 2022
Shaggag LM 2022 50 80 115 250 3.3% 1.96 [1.17, 3.28] 2022
Trivedi P 2022 37 80 143 1897 3.7% 10.55 [6.59, 16.91] 2022
Total (95% CI) 827223 1779366 100.0% 1.81 [1.60, 2.03]
Total events 104566 223093
Heterogeneity: Tau2 = 0.04; Chi2 = 558.99, df = 28 (P < 0.00001); I2 = 9 5%
Test for overall effect: Z = 9.73 (P < 0.00001)
Odds Ratio M-H, Random, 95% CI
0.02
0.1 10 50
Favours [control] Favours [experimental]
Figure 2 - Forest plots of summary crude odds ratios (ORs) and 95% confidence intervals (CIs) for the periodontitis and preterm birth.
Figure 3 - Funnel plot for assessment of potential publication bias.
Egger's test for potential publication bias in the included studies
Figure 1 - Flow diagram of the study search and identification.
Egger's test
Intercept 2.2885
95% CI 0.6757 to 3.9013
Significance level P = 0.0071
sections of the mother hematogenously, while these pathogens have been isolated from the placenta and amniotic fluid of preterm cases [39]. A most recent Israel study found that the high level of Gal-GalNAc, also known as Thomsen Friedenreich antigen during pregnancy mediates the placental colonization by Fusobacterium nucleatum [40].
Our study is limited by the inconsistent research design, as the includ studies regardless of the prospective and retrospective cohort and case control studies. Secondly, the unequal baseline of the sample in studies, such as geographic distribution, age, socio economic factors may also have influenced the heterogeneity of the studies, since most of the studies were carried out in the developed western countries. In addition, both health conditions share some major confounding factors, which may bias the estimates. In an attempt to minimize the possibility of publication bias, more databases were selected to search the original evidence. Furthermore, the diagnostic criteria for the periodontitis in the studies are difficult to standardize, while there are several diagnostic criteria presented in these studies and evaluated the association according to the definition used. In this sense, it is necessary to standardize criteria for determining periodontitis for pregnant women, which aims at greater methodological homogeneity between studies and
a more consistent direction for the clinical practice of dental professionals. Further validation or substantiation about the association needs to collect more robust data.
Conclusion
Periodontitis during pregnancy must be considered as one of the important factors which is associated with increased risks of preterm birth. It is important to put the disease under control before and during pregnancy while it is preventable and treatable. It may be important to reduce the preterm birth outcome.
Disclosures: There is no conflict of interest for all authors.
Acknowledgements: None.
Funding: The research funded by the project named "Gene-infection interaction in spontaneous preterm birth" by the Ministry of Science and Higher Education of the Republic of Kazakhstan (AP14972889) and "Clinical, Genomic and Environmental Variable Approach to Preterm birth" by the Ministry of Science and Higher Education of the Republic of Kazakhstan (AP14869249).
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