E‐cigarettes effect on periodontal health: a systematic review

231 Odonto : Dental Journal. Volume 9. Number 2. December 2022 E‐cigarettes effect on periodontal health: a systematic review I Komang Evan Wijaksana*, Ni Luh Ayu Megasari** * Department of Periodontology, Faculty of Dental Medicine Universitas Airlangga, Surabaya-Indonesia ** Postgraduate School, Universitas Airlangga, Surabaya-Indonesia Correspondence: [email protected] Received 23 May 2022; 1st revision 31 Augustus 2022; 2nd revision 24 October 2022; Accepted 2 November 2022; Published online 28 December 2022 Keywords: Electronic cigarettes; ecig; periodontal health; smoking; human and health ABSTRACT Background: Smoking is well known risk factors that promote periodontal tissue destruction. Both smoking and periodontitis nowadays consider as a common health problem globally. As smoking habit evolution, electronic cigarettes (E-cigs) have emerged as an alternative to cigarettes. The number of E-cigs smoker or vaping users around the world are increasing. However, information about the effect of E-cigs on periodontium is very lacking lately. The study aimed to compare the effect of cigarette consumption on periodontium by clinical health parameters between all smokers’ type. Method: This review follows the PRISMA guidelines. Document search was carried out in PubMed, Ebsco Host and Scopus using the keywords or phrases: (periodontal health) AND (((((electronic cigarette) OR Vaping) OR e-cig) OR electronic nicotine delivery system) OR nicotine delivery system). A total of 137 articles were obtained after the duplicates were eliminated and five articles were considered met the eligibility criteria for systematic review. Result: This review found that E-cigs are less harmful compared to tobacco cigarettes, with comparable result between E-cigs smoker and non-smoker on some clinical periodontal health parameters for mean probing depth, clinical attachment loss, score of plaque index (PI) and papillary bleeding index (PBI) as well. In contrast, the study reveals that bleeding on probing level was higher among non-smokers than smokers. Conclusion: E-cigs are less harmful compared to tobacco cigarettes on some clinical periodontal health parameters. This result should be interpreted with caution because there is currently insufficient data to investigate the effect of E-cigs on periodontal health through clinical parameters. Copyright ©2022 National Research and Innovation Agency. This is an open access article under the CC BY-SA license (https://creativecommons.org/licenses/by-sa/4.0/) doi: http://dx.doi.org/10.30659/odj.9.2.231-240 2460-4119 / 2354-5992 ©2022 National Research and Innovation Agency This is an open access article under the CC BY-SA license (https://creativecommons.org/licenses/by-sa/4.0/) Odonto : Dental Journal accredited as Sinta 2 Journal (https://sinta.kemdikbud.go.id/journals/profile/3200) How to Cite: Wijaksana et al. E‐cigarettes effect on periodontal health: a systematic review. Odonto: Dental Journal, v.9, n.2, p.231-240, December 2022 Wijaksana/ Megasari INTRODUCTION 232 periodontal tissue, are rarely reported in the Smoking-related diseases are a well-known literature.3 public health issue that affects people all over the The use of E-cigs are increasing around the world.1–3 According to WHO data, the smoking world, but more research into its effect on prevalence among people aged 15 years in high periodontal tissue is needed. On that basis, the income countries is expected to be 22.4% in 2020 purpose of this systematic review was to examine and 20.5% in 2025 for both sexes. In the meantime, the current evidence and compare the effect of E- WHO projected 22.4% and 20.5% for upper middle- cigs and other types of smokers on periodontal income countries, against the 10.7% and 9.8% for tissue health using available clinical parameters. the low-income countries. The projected data show a decrease from 2020 to 2025, but WHO estimates LITERATURE REVIEW that 10% of deaths in 2020 will be caused by Data Selection smoking.4 As a result, smoking has become one of the world's major public health issues.2,5 The guidelines for PRISMA (Preferred Reporting Items for Systematic Reviews and Meta- Periodontal diseases are oral disease that analysis) are based on the results of this systematic ranks first in the 2001 world book record as a review. We set a review question based on the common disease that is often found in the PICO strategy: "Will E-cigarette smokers (ES) have community.6 high a better clinical periodontal health parameter when prevalence, is known as major global oral health compared to non-smokers (NS) and smokers?". problem. Periodontitis can negatively affect the Smokers were designated as the population (P), ES tooth supporting structure lead to a decreasing of as the intervention (I), and NS, conventional periodontal support to the teeth, impairing tooth smokers (CS), or other types of smokers as the function on mastication and also facial aesthetic, comparison (C), with clinical periodontal health as being the initial source of systemic infection and of the outcome (O). Periodontitis, due course impairing the host quality of to its life. 7–9 Study from 1990-2010 showed that severe periodontitis was the sixth highest prevalence of the disease (11.2%) with an increase in prevalence of 57.3% in 10 years.6,10 Smoking is well known risk factors that promote periodontal tissue destruction.11 Both smoking and periodontitis nowadays consider as a common health problem globally.7,12 Some countries now have laws that regulate and limit tobacco use in public places. Electronic cigarettes (E-cigs) have emerged as a popular alternative to cigarettes among adolescent smokers for the first time or former smokers who prefer Ecigs to be used for smoking cessation. The effects of E-cigsor vaping on oral health, particularly Odonto : Dental Journal. Volume 9. Number 2. December 2022 Identification 233 E‐cigarettes effect on periodontal health: a systematic review PubMed (n= 32) Ebsco Host (n= 63) Scopus (n= 56) December 24th, 2020. Observational or analytical studies that evaluated at least one clinical periodontal health parameter were included in the review. Exclusion criteria for the study included an article review, cell and/or animal studies, and questionnaire-based studies. Screening Data after duplicates removed (n= 137) Two independent authors manually removed the duplicate references using a Microsoft Excel 2016 spreadsheet (Microsoft USA). The initial Data excluded (n= 130) Data screened (n= 137) selection was done through titles and abstracts, and the final quality checks on the studies included in the final review were done by independent authors Eligibility using the ROBIN-I methodological index, which Articles that assessed for eligibility (n= 7) Articles excluded, with reasons (only applied questioner (n= 2)) followed the same guidelines as Ralho et al.3 Result In the initial literature search, 151 articles Included were discovered, with 32 articles coming from Studies included in final synthesis (n= 5) PubMed, 63 from Ebsco Host, and 56 from Scopus. After removing duplicates, a total of 137 articles were obtained, of which 7 were chosen through title and abstract screening. Five articles were considered eligible for the final systematic review Figure 1. Flowchart of article selection according to PRISMA, five articles were considered met the eligibility criteria for final review. (Figure 1). All of the articles included in the systematic review were published between 2016 and 2020. An Internet search was conducted in PubMed, Ebsco Host, and Scopus using the keywords or phrases: (periodontal health) AND (((((electronic cigarette) OR Vaping) OR E-cigs) OR nicotine delivery system) OR electronic nicotine The studies included in the systematic review were classified into four types: case control studies 13,14, cross-sectional observational studies15, a pilot cross over study design16, and clinical observational pilot studies1. delivery system) OR electronic nicotine delivery system) with full text filters for the 2010-2020 document. The most recent search took place on Odonto : Dental Journal. Volume 9. Number 2. December 2022 Wijaksana/ Megasari 234 Table 1. Demography of the studies eligible for the final review Parameter Author Javed et al., 2017 13 BinShabaib et al., 2019 Sample Subjects Number Male: NS 30 30:0 40.7 ± 1.6 - - - 23.3 ES 31 31:0 37.6 ± 2.1 2.2 ± 0.2 6.8 ± 0.8 NI 60.6 CS 33 33:0 41.3 ± 2.8 5.4 ± 1.6 13.3 ± 2.6 NI 68.5 NS 45 39:6 40.6 ± 3.3 - - - NI ES 44 42:2 36.5 ± 1.7 9.4 ± 2.6 NI 20.3 ± 3.5 NI CS 46 43:3 44.2 ± 3.5 14.2 ± 0.6 NI 5.2 ± 0.6 NI NS 38 38:0 40.6 ± 4.5 - - - 28.9 ES 37 37:0 28.3 ± 3.5 3.1 ± 0.4 9.2 ± 1.4 8.1 ± 1.3 27.0 CS 39 39:0 42.4 ± 5.6 17.2 ± 2.5 16.2 ± 2.5 4.8 ± 0.3 58.9 WS 40 40:0 44.7 ± 4.5 14.6 ± 5.7 4.3 ± 0.5 17.1 ± 3.4 67.5 ES 18 NI 18-65 NI NI NI NI CS 19 NI 18-65 NI NI NI NI ES1 60 NI NI NI NI 89:21 31 ± 9 NI NI NI NI Female Age in years (mean ± SD) Duration of smoking habit (in years) Daily frequency of habit Duration of each session in minutes (mean ±SD) Family history of smoking (%) 15 Mokeem et al., 2018 14 Wadia et al., 2016 16 Tatullo et al., 2016 1 ES2 50 CS (Conventional Cigarette Smoker); ES (Electronic Cigarette Smoker); ES1,2 (ES group 1,2); NA (No Information); NS (Non-Smoker); WS (Waterpipe Smoker) The demographics of the included studies while moderate risk was applied for biases in (table 1) showed a total of 530 subjects from all participant selection due to possibly biases.14 There included studies. Except for Wadia et al (2016) all was a low risk of bias in reviewer judgment for the studies that specified the gender of subjects were intervention postintervention phases. included16, . The subjects of included studies were Five clinical parameters were recorded on 461 males and 32 females. Two studies13,14 studies to assess periodontal health: bleeding on included only male subjects. The subjects' ages probing (BoP) score, probing depth (PD) score, ranged from 18 to 65 years old. clinical attachment loss (CAL) score, plaque index The risk of bias assessment (table 2) was (PI) score, and the last papillary bleeding index performed as part of the quality assessment for (PBI) score. PI was evaluated in all of the studies studies that were eligible for the final review. For that were included. Except for Tatullo et al.,1 all each risk of bias parameter, the quality assessment studies evaluated BoP, PD, and CAL. was graded using a five-point scale: Y (Yes), PY Table 3 summarizes the findings from the five (Probably Yes), N (No), PN (Probably No), and NI studies that qualified for the final review. Because (No Information). For the Mokeem et al (2018), of the disparity in methodology and clinical study, reviewer judgement for pre-intervention parameters assessed in the included studies, biases including confounding biases was low risk, Odonto : Dental Journal. Volume 9. Number 2. December 2022 235 E‐cigarettes effect on periodontal health: a systematic review quantitative analysis on this systematic review was not possible. Table 2. Quality assessment for risk of bias of the studies included in final review. At Pre-intervention Post-intervention intervention Risk of bias parameter Studies confounding selection of participants into the study interventions classification intended interventions deviations missing data outcomes measurement reported result selection PN N N N N PN N N N N N N N N Mokeem et al., 2018 14 PN PY N N N PN N Wadia et al., 2016 16 PN N N N N PN N Tatullo et al., 2016 1 PN N N N N N N Low risk Low risk Low risk Low risk Javed et al., 2017 13 BinShabaib et al., 2019 15 Risk of Moderate Bias Low risk Low risk risk Judgement PY (Probably Yes), N (No), PN (probably No) Odonto : Dental Journal. Volume 9. Number 2. December 2022 Wijaksana/ Megasari 236 Table 3. E-cigs effect on periodontium by clinical health parameter Clinical Periodontal Health Parameter Evaluated Subject Author Study type Sample CAL criteria (mm) BoP (%) PD (%) PI (%) PBI 1. CS (Daily NS ≥4mm: 27.5±3.2 0.8±0.1 21.4±2.8 NA frequency (n=30) 29.3±1.7 ES ≥4mm: ≥5 cig/day 4.6±2.9* 1.1±0.2 23.3±3.4 NA (n=31) 5.1±1.2 ≥1 year); Case 2. ES (Using Javed et control ≥1 year al., 2017 13 study ≥4mm: without CS 52.1±6.6* 5.8±0.8* 2.1±0.2 NA 29.3±1.7* † (n=33) tobacco † use); 3. NS 1. CS (Daily 28.4b 18.2 NS 1.6 (1.2– 0.6 (0.5– frequency (26.3– (23.5– NA (n=45) 2.2) 1.2) ≥5 cig/day 33.4) 34.3) cross≥1 year); BinShabai 12.2 33.4 sectional ES 2.5 (2.2– 1.7 (0.5– 2. ES (Just NA b et al., (14.4– (29.6– observation (n=44) 3.4) 1.4) using E-cigs 2019 15 20.5) 39.7) al study at least 10.6 42.1a CS 5.3a (4.4– 2.8a 1/day); (15.5(40.3– NA (n=46) 6.3) (1.8–3.1) 3. NS 22.4) 46.3) 1. CS (Daily NS Referenc Referenc Referenc Reference NA frequency (n=38) e e e ≥5 cig/day ES ** ND ND ND NA ≥1 year); (n=37) Mokeem Case 2. ES (≥1 CS et al., control a a ** ** NA year); (n=39) 2018 14 study 3. WS (≥1/day WS a a ≥1 year); ** ** NA (n=38) 4. NS 1. CS (Daily ES ND NA NA frequency (n=18) ≥10 cigarettes/ CS day ≥5 Wadia et A pilot cross significantl ND years), then al., 2016 over study y higher 16 CS 2 replaced design NA NA than ES (n=18) ±0.43mm smoking habits to Ecig for 2 weeks (ES). T0: T0: 0.9±0.3 0.4±0.49 1. ES ES1 (n= NA NA NA T1: T1: approximatel 60) 0.8±0.4 0.2±0.4 Clinical y from 4±1 observation T2: 0 T2: 0 month al pilot T0: 2. ES1 (< 10 T0: study (120 Tatullo et 1.25±1.3 years of 2.13±0.5 al., 2016 1 days with 3 4 tobacco different T1: smoking) ES2 (n= T1: check0.25±0.4 NA NA NA 3. ES2 (> 10 50) 1.63±0.7 points) 5 years of T2: tobacco 0.25±0.4 T2: 0 smoking) 5 BoP (Bleeding on Probing); CAL (Clinical Attachment Loss); CS (Conventional Cigarette Smoker); ES (Electronic Cigarette Smoker); NA (Not applicable); ND (Not significantly different); NS (Non-Smoker); PBI (Papillary Bleeding Index); PD (Probing Depth); PI (Plaque Index); T012 (first, second and third checkpoint); WS (Waterpipe Smoker); * Significant difference compared with group NS (P<0.01); ** Significant difference compared with group NS (P<0.05); † Significant difference compared with group ES (P<0.01); a Compared with Group ES (P < 0.05) and Group NS (P < 0.05); b Compared with Group CS (P < 0.05) and Group ES (P < 0.05). Odonto : Dental Journal. Volume 9. Number 2. December 2022 237 E‐cigarettes effect on periodontal health: a systematic review vasoconstrictive effect on gingival blood vessel.1,28 DISCUSSION Adolescent’s general perception of E-cigs compared to conventional cigarettes is considered to be less harmful17 and less addictive18,19. Escalating use of E-cigs may be partly due to public perception about E-cigs are less harmful dan smoke cigarettes.20–24 Most of former smokers’ belief that by using E-cigs, they are less risky, and can be a substitute and helpful for cigarettes smoking cessation,25,26 and this systematic review confirms that believe. This review found that E-cigs are less harmful compared to tobacco cigarettes, with comparable result between E-cigs smoker and non-smoker on some clinical periodontal health parameters for mean probing depth, clinical attachment loss, score of plaque index (PI) and also papillary bleeding index (PBI). In contrast, the study reveals that bleeding on probing level was higher among nonsmokers than smokers. This result should be interpreted with caution because there is currently insufficient data to investigate the effect of E-cigs on periodontal health through clinical parameters. Bleeding on probing (BoP) is one of the fundamental clinical parameter health for periodontium. BoP related to early sign of clinical inflammation on periodontium. BoP can be found in early lesion of gingivitis and can be visualized earlier than redness and swelling.27 Three studies reported that BoP site significantly higher in NS subjects comparing to ES or CS with no differences between ES and CS.13–15 Study by Wadia et al. (2016) reported that when subject switch the smoking habit from CS to ES, the number of BoP site are increased.16 Subject who was waterpipe smoker has a lower BoP site compared to nonsmoker as reported by Mokeem et al.14 Nicotine, which found in tobacco cigarette and E-cigs liquid, has known to decreasing the gingival bleeding response due to its This vasoconstriction effect also impairing the gingival crevicular fluid (GCF) by decreasing the GCF flow rate. Thus, potentially impairing the homeostasis between host response to intraoral microbiome. Nicotine is also known to reduce cellular healing potential.1,3 ES just like CS may unaware of oral inflammatory change escalation due to less perceptible of bleeding on their periodontium compared to non-smokers.3 Another bleeding parameter was Papillary Bleeding Index (PBI). Out of five study included in review, only Tatullo et al.,1 showing the parameter of PBI. Tatullo et al.,1 showing when CS switched to ES, there are constant reduction of PBI. Subject with more than 10 years of tobacco smoking habit (ES2) have a marked reduction of PBI when compared from initial (T0) to the last observational period (T2). Probing depth (PD) and clinical attachment loss (CAL) alone are insufficient indicators of periodontal health or disease because they are insufficient parameters to predict the sites with potential infection or experience of disease recurrency. However, both PD and CAL can be useful when combined with BoP information.27 A significant higher PD in CS were observed by three studies compared to ES and NS, while no difference between ES and NS.13–15 When smokers switch from CS to ES, no differences in PD were observed.16 However, must be noted that in Wadia et al.(2016) ,studies, the initial mean of PD was 2 ±0.43mm and included sample has PD ≤4 mm at any site. 16 . In terms of CAL, only Javed et al. (2017) not found that CAL is higher in CS than in ES and NS.13 Nicotine consumption both the frequency and duration was nearly twice as high among CS as it was among ES.13 . This study demonstrated that CAL are insufficient evidence of periodontal health Odonto : Dental Journal. Volume 9. Number 2. December 2022 Wijaksana/ Megasari 238 or disease. Previous research has also confirmed or frequency of smoking. Third, quantitative that CS have a significantly higher number of PD analysis is not possible due to differences in and CAL than NS.29–31 Tobacco smoking is methodology and clinical parameters assessed in associated with an increase in advanced glycation the studies. Further research is needed to evaluate end this theme, allowing the use of strict inclusion and products (AGEs) and their receptors expression in oral epithelial cells, including gingival exclusion criteria. tissues, which exacerbates oxidative stress and inflammatory responses.13,21 Smokers are known to have a lower salivary flow rate and GCF compared to non-smokers. To confirm that condition, Plaque index (PI) will be useful parameter. PI is primarily associated with plaque control as well as adequate salivary and crevicular fluid flow. Variations in PI score may be due to differences in salivary and GCF flow rate between groups.1,3,32 This review confirm that CS has poorer PI compared to ES and NS.13–15 Tatullo et al. (2016) CONCLUSION Within the scope of the current study, it is concluded that clinical periodontal health parameters are better in E-cigs smokers than in other smoker groups, and that E-cigs smokers may have periodontal status comparable to nonsmokers besides BoP level. However, E-cigs should not be considered a risk-free alternative. CONFLICT OF INTEREST No conflict of interest and financial demonstrated that when CS was switched the disclosures were reported by the authors of this habits to ES, there was a consistent reduction of PI paper. from baseline to T2 as the end of observational period, which found more pronounced in group ES2 who had a high PI score at T0.1 In contrast, Wadia et al. (2016) found no difference when CS was replaced with ES.16 ACKNOWLEDGMENTS This work was supported by Faculty of Dental Medicine Universitas Airlangga Surabaya. In this case, different observational periods may affect the outcome. REFERENCES Wadia et al. (2016) observed the outcome after two 1. 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