Electronic Cigarettes, Heated Tobacco Products, and Oral Health: A Systematic Review and Meta-Analysis
Abstract
:1. Introduction
- The respiratory system (cough, asthma and bronchitis);
- The cardiovascular system (heart rate and blood pressure increase);
- The oropharyngeal system (oral cavity and pharynx lesions);
- Skin and annexes (dermatitis);
- Second-hand smokers or passive smokers (increased cotinine levels);
- Other (headache, eye problems due to vapor and glycerol, burns and lacerations).
2. Materials and Methods
2.1. Study Registration
2.2. Reporting Format
2.3. Population (P), Exposure (E), Comparison (C), Outcomes (O), and Study Design
2.4. Inclusion Criteria
- Interventional and observational studies on ENDS and HTP and their effects on oral health;
- Studies including subjects of any age or sex;
- Full and/or pilot studies reporting data;
- For the laboratory studies, articles considering human oral cells or oral bacteria;
- Studies in English, without time limits.
2.5. Exclusion Criteria
- Systematic or narrative reviews and meta-analyses;
- Theses and dissertations;
- Case reports/series;
- Studies reporting insufficient/unclear information, or not allowing data extraction;
- Papers not published in English;
- Papers focused on different aspects of health other than oral health;
- Studies for which the authors did not respond to the email requesting data clarification.
2.6. Search Strategies
2.7. Electronic Search
2.8. Manual Search
2.9. Study Selection
2.10. Data Extraction and Variable Analysis
2.11. Risk of Bias
2.12. Synthesis of the Results
2.13. Subgroup Analyses
2.14. Sensitivity Analysis
2.15. Unit-of-Analysis Issues
Authors, Year (Country) | Total N of Participants (% Male); N of Participants in Each Group | Outcome | Aim | Conclusion |
Study Design | Age (Years) | |||
Part A—Studies with Clinical Examination | ||||
Al Aali et al., 2018 (Saudi Arabia) [28] Cross-sectional with clinical examination | 92 (100) EC: 47, NS: 45 YA | BOP, PPD, biomarkers, X-rays | Compare clinical and X-rays peri-implant parameters and levels of TNF-a and IL-1b levels among ECS and NS | Clinical, microbiological, and radiographic peri-implant parameters are compromised among ECS. |
Alazmi et al., 2021 (Saudi Arabia) [29] Cross-sectional with clinical examination | 127 (72); ECS 63, NS 64 YA | Peri-implant CBL, PD, PI, BOP, X-rays, and self-reported OH status and practice | Assess peri-implant parameters at 8 years follow-up | Implants of ECS and NS exhibited clinical and radiographical status when at home OH practice was good. |
Ali et al., 2022 (Kuwait) [30] Cross-sectional with clinical examination | 75 (21); ECS 18, CS 19, NS 38 MA | PPD, PI, GI, CAL, MBL, IL, whole saliva | Compare the periodontal status and saliva, IL-15, and -18 levels among CS, ECS, NS | Clinically, CS and NS demonstrate similar periodontal statuses; IL and salivary parameters are more elevated in smokers. |
AlQahtani et al., 2018 (Saudi Arabia) [31] Cross-sectional with clinical examination | 160 (100); ECS: Age: 42 YA | BOP, PI, PPD, biomarkers | Compare clinical and radiographic peri-implant parameters and proinflammatory cytokine profile in the peri-implant sulcular fluid among the groups | ECS and OS (waterpipe) users may be at risk of poor peri-implant health. Tobacco smoking is associated with poor peri-implant health. |
AlQahtani et al., 2019 (Saudi Arabia) [32] Cross-sectional with clinical examination | 137 (100); ECS: 34, CS: 35, OS: 33, NS: 35 YA | Cotinine levels at peri-implant BOP, PI, PD, biomarkers | Compare cotinine levels in the peri-implant sulcular fluid among the groups | Cotinine levels in the peri-implant sulcular fluid of cigarette and OS (waterpipe) smokers and electronic-cigarette users are comparable. |
Alqahtani et al., 2022 (Saudi Arabia) [33] Cross-sectional with clinical examination | 150 (12); ECS 50, CS 50, NS 50 YA | Community periodontal index treatment need | Evaluate the periodontal treatment needs among CS, ECS, and NS | CS require more complicated periodontal treatment compared to ECS. |
ArRejaie et al., 2019 (Saudi Arabia) [34] Cross-sectional with clinical examination | 95 (100); ECS: 31, CS: 32, NS: 32 YA | BOP, PI, PPD, CAL, MBL, biomarkers (MMP, IL), X-rays | Compare clinical and radiographic peri-implant parameters and biomarkers among CS, ECS, and NS | Peri-implant health was compromised among CS than ECS and NS. Increased levels of proinflammatory citokines were found in CS and ECS. |
Bardellini et al., 2018 (Italy) [35] Prospective case-control | 90 (71); FS: 45, EC: 45 MA | Oral mucosal lesions | To evaluate the prevalence and characteristics of OMLs in FS compared to ECS | No statistically significant differences regarding total prevalence of OMLs between FS and ECS. Nicotine stomatitis, hairy tongue, and angular cheilitis were significantly more common among ECS. |
Binshabaib et al., 2019 (USA) [36] Cross-sectional with clinical examination | 135 (92); CS: 46, ECS: 44, NS: 45 YA | BOP, PI, PPD, X-rays, biomarkers | Compare the clinical periodontal status and gingival crevicular fluid (GCF) cytokine profile among CS, ECS, and NS. | Periodontal status is poorer and GCF levels of proinflammatory cytokines are higher in CS compared with ECS and NS. |
Dalrmyple et al., 2022 (Germany) [37] Pilot study—cross-sectional | 33 (45); ECS 11, CS 11, NS 11 | Breath odor | Determine differences in breath odor between ECS, CS, and NS | ECS breath has a reduced smoke odor and more pleasant aroma than CS, and is comparable to NS. |
Ghazali et al., 2019 (Malasya) [38] Cross-sectional with clinical examination | 135 (99); CS: 45, ECS: 45, NS: 45 EA, YA, MA | DMFT | Evaluate caries experience among CS, ECS, and NS | CS and ECS have potential detrimental effect on caries development. |
Herndon et al., 2022 (USA) [39] Cross-sectional questionnaire with clinical examination | 4544 (48); current ECS: 260, no current ECS: 4284 EA, YA, MA, OA | Self-reported OH | Recall of ECS for HPV test | E-cigarette use increases the persistence of HPV infection. |
Ibraheem et al., 2020 (Saudi Arabia) [40] Cross-sectional with clinical examination | 120 (100); ECS: 30, CS:30, NS: 30, OS: 30 MA | BOP, PI, PPD, X-rays, NF-kappa B ligand | Compare the levels of receptor activator of NF-kappa B ligand (RANKL) and osteoprotegerin (OPG) in the GCF of the groups | CS and OS (waterpipe) and ECS usage is associated with an increased expression of RANKL and OPG in the GCF. |
Javed et al., 2017 (USA) [41] Cross-sectional questionnaire and clinical examination | 94 (100); ECS: 31, CS: 33, NS: 30 YA | Self-reported OH status PI, GI, PPD, CAL, biomarkers | Assess periodontal parameters and self-perceived OH | Periodontal inflammation and self-perceived OH are exacerbated in CSS compared with ECS and NS. |
Jeong et al., 2020 (South Korea) [42] Cross-sectional questionnaire and clinical examination | 13,551 (58); ECS: 222, NS: 8342, CS: 2330, FS: 2667 EA, YA, MA, OA | Self-reported OH status | Self-report periodontal status, community periodontal index | The results of the current study could motivate both ECS and CS to quit by highlighting the association of conventional cigarette smoking and electronic cigarette vaping with periodontal disease. |
Karaaslan et al.2020 (Turkey) [43] Cross-sectional with clinical examination | 57 (68); ECS: 19, CS: 19, FS: 19 YA | PI, GI, PD, CAL, MBL, biomarkers | Effects of smoking on oxidative stress markers, proinflammatory cytokines levels, and periodontal clinical parameters in patients with periodontitis | Vaping ECS and CS had the same unfavorable effects on the markers of oxidative stress and inflammatory cytokines. |
Mokeem et al., 2018 (Saudi Arabia) [44] Cross-sectional with clinical examination | 154 (100); CS: 39, OS: 40, ECS: 37, NS: 38 YA | PPD, PI, BOP, CAL, X-rays | Compare periodontal index and biomarkers among smokers and NS | Clinical and radiographic parameters of periodontal inflammation were poorer in CS and OS (waterpipe) than ECS and NS. |
Tatullo et al., 2016 (Italy) [45] Cross-sectional questionnaire and clinical examination | 110 (81) ECS: 110 (all former CS) YA | Self-reported need to smoke PI, BI, PBI | Verify the clinical variations of periodontal health induced by EC and investigate the awareness of ECS about their health variations and need to turn back to CS | E-cigarette can be considered as a valuable alternative to tobacco cigarettes, with a positive impact on periodontal and general health status. |
Vohra et al., 2019 (USA) [46] Cross-sectional questionnaire and clinical examination | 105 (100); CS: 28, ECS: 51, NS: 26 YA | Self-reported OH BOP, PI, PPD, CAL | Compare self-rated oral symptoms with periodontal status | Pain in teeth and gums is more often perceived by CS than ECS and NS. CS is more associated with increased PI and PD than is ECS. |
Part B—without Clinical Examination | ||||
Akinkugbe 2019 (USA) [47] | 13,650 (50); current ECS 418, current CS 634, Other 12,598 | Self-reported OH status and OH practice—PATH | Epidemiology of dental status of CS and ECS among adolescents | Dual users are associated with poor oral health outcomes. |
Cross-sectional questionnaire | EA | |||
Alade et al., 2022 (Nigeria) [48] | 2870 (51); CS 378, ECS 167, DS 401, NS 1916 | Self-reported oral lesions | Effects on OH for different smokers who had COVID-19 infection | ECS had 1.5 times higher odds of reporting oral lesions than NS. Those who had COVID-19 infection had higher odds of gingivitis. |
Cross-sectional questionnaire | MC, EA, YA | |||
Alhajj et al., 2022 (Yemen) [49] Cross-sectional questionnaire | 5676 (40); ECS 255, CS 596, DS 261, NS 4565 YA, MA | Self-reported OH status and OH practice | Assess self-reported OH practices and events in ECS | ECS reported more oral health-related conditions, particularly xerostomia and black tongue, and heart palpitation. |
Alqobaly et al., 2022 (UK) [50] Cross-sectional questionnaire | 8129 (48); erce data not applicable MA | Self-reported periodontal status | Assess self-reported periodontal disease in ECS | ECS use is associated with self-reported periodontal disease. |
Atuegwu et al., 2019 (USA) [51] Cross-sectional questionnaire | 32,320 (46), in 3 waves of survey; NS: 9632, regular ECS: 329, non regular ECS: 8298 EA, YA, MA, OA | New cases of gum disease in 12 months | Assess the association between ECS and PD | ECS may be harmful to OH. |
Ho Cho et al., 2017 (South Korea) [52] Cross-sectional questionnaire | 65,528 (52); ECS: 1556, Former ECS: 3848, Never ECS: 60,124 EA | Oral symptoms (Gingival pain/bleeding, tongue or cheek pain, cracked or broken teeth) | Assess the relationship between EC use and OH | ECS among adolescents may be a risk factor for tongue and/or inside-cheek pain and cracked or broken teeth. |
Huilgol et al., 2019 (USA) [53] Cross-sectional questionnaire | 456,343 (43); ECS: 15,019, Non ECS: 441,324 EA, YA, MA, OA | Self-reported poor OH symptoms | Assess the ECS use on OH | Daily use, but not intemittent use, of ECS was independently associated with poor OH. |
Irusa el al; 2022 (USA) [54] Cross-sectional questionnaire | 13,080 (48); ECS 136, Other 12,944 EY, YA, MA, OA | Caries risk | CAMBRA tool (the caries management from risk assessment) | ECS had higher caries risk than non-ECS. |
Abafalvi et al., 2018 (Hungary) [55] Cross-sectional questionnaire | 930 (83) ECS: 767, DS: 163 EA, YA, MA, OA | Self-reported oral hygiene practice | Assess self-reported oral hygiene practice among ECS and DS | Both groups showed inadequate oral hygiene practices. |
Vemulapalli et al., 2021 (USA) [56] Cross-sectional questionnaire | 4618 (48); EC: 247, FS: 700, NS: 3671, DS:120, Former DS: 561 EA, YA, MA | Untreated caries | Examine the association between ECS and untreated caries | Both ECS and DS are associated with an increased occurrence of untreated caries. |
Vora et al., 2019 (USA) [57] Cross-sectional questionnaire | TOT: 32,300 (48) ECS: 97, NS: 9076, CS: 4231, FS: 14,115, OS: 4748 EA, YA, MA | Self-reported OH status | Evaluate self-reported gum disease among ECS and other types of smokers | Numerous tobacco use patterns were associated with worse periodontal health compared to NS. |
Yoshioka et al., 2022 (Japan) [58] Cross-sectional questionnaire | TOT 10,439 (54) 1034 CS, 437 heated tobacco products, FS 1853, 1049 DS, NS 5796 EA, YA, MA, OA | Self-reported history of PDis | Compare self-reported periodontal disease among smokers and NS | All the smokers were significantly associated with a higher prevalence of periodontal diseases compared to NS. |
Authors, Year Country, Study Design | Sample (%Male) Age Category | Outcome and Parameters | Aim | Conclusions |
---|---|---|---|---|
Akram et al., 2021 (Australia) [59] Longitudinal, three observations: 3 m, 6 m | TOT: 60 (100) ECS: 30, CS: 30 YA, MA | PPD, BOP, CAL periodontal disease, biomarkers | Evaluate the periodontal parameters and MMP-8 and CTX in ECS and CS | CS showed an increased periodontal worsening compared to ECS. |
Al Deeb et al., 2020 (Saudi Arabia) [60] Randomized controlled clinical trial 3 observations: BL, 2 w 12 w | TOT: 71 (100) ECS: 21, CS: 25, NS: 25 Age: YA | BOP, PPD, PI, biomarkers | Effectiveness of PDT AAOAN adjunctive therapeutic modality in the treatment of peri-implant mucositis for ECS and CS | PDT with adjunctive mechanical debridement reduced PI and PD, while increasing BOP, in addition to reducing pro-inflammatory biomarkers CS. |
Al Hamoudi et al., 2020 (Saudi Arabia) [61] Longitudinal, two observations, BL, 3 m | TOT: 71 (88) ECS: 36 Age: 47 YA, MA | GI, PPD, CAL, X-rays, GCF, IL | Periodontal parameters pre-post SRP | Levels of GCF IL-4, IL-9, IL-10, and IL-13 increased following SRP in ECS and NS with CP; the anti-inflammatory effect of SRP was more profound in NS. |
Al Harti. 2019 (Saudi Arabia) [62] Prospective | TOT: 89 (100) ECS: 28, CS: 30, NS: 31 Age: 34 YA | BOP, PI Percentage of CS and EC on periodontal tissues after FMUS | After FMUS, gingival inflammation is worse in CS compared with ECS and NS. | |
Alhumaidan et al., 2022 (Saudi Arabia) [63] Longitudinal, two observations BL, 3 m | TOT: 54 (67) ECS: 18, CS 18, NS 18 YA | CAL, Mt, PDis, PI, and MBL, percent vary cortisol | Evaluate salivary CL and IL-1β levels in light CS and ECS users before and after non-surgical periodontal therapy | In CS and ECS, users without Pdis, clinical periodontal parameters and whole-salivary CL and Il-1β levels remain unchanged after non-surgical periodontal therapy. |
AlJasser et al., 2021 (Saudi Arabia) [64] Longitudinal, four observations BL, 3 m, 6 m, 12 m | TOT: 60 (52) ECS: 20, CS 20, NS 20 MA | BOP, PI, PD, IL | Compare changes in clinical periodontal parameters and changes in salivary IL between CS, ECS, NS after peri-implant treatment | Electronic cigarette smoking was found to be a mercentagelent risk indicator for peri-implantitis. |
AlRifaiy et al., 2018 (Saudi Arabia) [65] Randomized controlled clinical trial 2 observations BL, 3 m | TOT: 38 (100) ECS with PDT: 20 ECS without PDT: 18 YA | BOP, PI, PrD, MBL | Effectiveness of antimicrobial therapy and PDT or erconly in ECS with p-iM | Antimicrobial PDT is more effective compared to MD alone in the treatment of p-iM in ECS. |
Alshibani et al., 2022 (Saudi Arabia) [66] RCT | TOT: 23 ECS Age not reported | CAL, PI, BOP, PPD, | Assess the effect of non-surgical periodontal therapy with adjunct photodynamic treatment for the management of periodontal inflammation in ECS | Photodynamic treatment is as effective as non- surgical therapy for the management of periodontal inflammation in ECS. |
Reuther et al., 2016 (UK) [67] Pilot clinical trial, two observations BL, 30 min | TOT: 10 volunteers who vaped EC specifically for the trial (70) YA | Blood flow in oral mucosa | Blood flow after vaping measured with Doppler laser | EC may have an effect on blood flow in the oral mucosa. |
Wadia et al., 2016 (UK) [68] Pilot longitudinal, two observations BL, 2 w | TOT: 20 switchers from CS to ECS EA, YA, MA, OA | BOP and GCF parameters | Compare the gingival health of a group of switcherercentagementage of sites with BOP increased statistically significantly 2 weeks after the switch. | |
Xu et al., 2021 (China) [69] Longitudinal, two observations BL, 6 m | TOT: 101 (71) ECS: 32, CS: 31, NS: 38 YA | PPD, BOP, CAL, saliva sample | Evaluate the adverse effects of vaping on periodontal health | Periodontal severity status after 6 months was significantly worse in CS and ECS than NS. |
Pouly et al., 2022 (Switzerland) [70] Randomized controlled clinical trial 3 observations BL, 3 m, 6 m | TOT: 172 (81) CS: 84, DS: 17, HTP: 70, Other: 1 YA, MA, OA | PPD, BOP, CAL, GI, PI | PD after scaling and root planingin smokers who switched or did not to HTP. | Scaling and root planing improves the course of PD similarly in CS and HTP. The treatment may mask favorables Pdis changes in the switchers. |
Authors, Year Country, Sub-Section | Cell line/Strain/Teeth/Sample | Outcome | Aim and Exposure | Conclusion |
---|---|---|---|---|
Alanazi et al., 2019 Canada [71] Oral Candida | Gingival epithelial cells | C. albicans activity | Impact on C. albicans growth and expression of different virulent genes Exp: ECS | EC may interact with C. albicans to promote their pathogenesis, which may increase the risk of oral candidiasis in e-cigarette users. |
Alanzi et al., 2018 Canada [72] Periodontology | HGF | HGF proliferation, migration, and apoptosis | Effects on HGF Exp: ECS ± nicotine and CS | Exposure to CS and EC negatively modulates gingival fibroblast activities. |
Aldakheel et al., 2020 Saudi Arabia [73] Periodontology | Subgingival oral biofilm sample from CS, ECS, NS | Quantity of pathogenic bacteria | Compare and quantify pathogenic bacteria from ECS, CS, NS, with and without periodontitis | Counts of periodontopathogen bacteria in the subgingival oral-biofilm are comparable among CS and ECS. |
Alzoubi et al., 2020 Giordania [74] Oral microbioma | Nasal and oral swabs from ECS, CS, NS | Microbial profile from ECS, CS, NS | To examine the oral and nasal microbial profile and antibiotics susceptibility in the ECS, CS, NS | ECS might be less harmful to microbiota compared to CS. |
Catala-Valentin et al., 2022 USA [75] Oral microbioma | S. sanguinis, S. gordonii, S. mutans | Bacterial growth | The effect on the growth of S. mutans, S. sanguis, S. gordonii the formation of biofilm, Exp: ECS | ECS exposure hinders S. sanguis and S. gordonii growth while enhancing biofilm formation, hydrophobicity, and attachment for S. mutans. |
Catala-Valentin et al., 2022 USA [76] Oral microbioma | S. aureus | Bacterial growth and oral epithelial cells deregulation | S. aureus attachment to oral epithelial cells and bacterial biofilm formation Exp: ECS | ECS promote S. aureus colonization and modulate the oral inflammatory response, possibly promoting oral periodontitis and preneoplasia. |
Chopyk et al., 2021 USA [77] Oral microbioma | Saliva, oral mucosa cells | Oral microbiome changes | Comparative analysis of the microbial community profiles Exp: ECS, NS | There are notable differences in the oral bacterial community composition and diversity in EC users as compared to the controls. |
Cicho’nska et al., 2019 Poland [78] Other | Salivary sample from ECS, CS, NS | Chemical property of saliva | Asses if ECS have an influence on selected antibacterial properties of saliva | Saliva of ECS showed changes in antibacterial properties in comparison to the NS and CS. |
Cicho’nska et al., 2021 Poland [79] Other | Salivary sample from ECS, CS, NS | Antioxidant capacity and nucleotide metabolites in saliva | Assess if ECS influence the antioxidant capacity of saliva | ECS affects antioxidant capacity of saliva to the same extent as CS, when comparing smokers to NS. |
Cicho’nska et al., 2022 [80] Poland Other | Salivary sample from ECS, CS, NS | Physicochemical properties of saliva (pH, protein, calcium phosphates) | Assess the impact of ECS on selected physicochemical properties of saliva | Saliva of ECS presents changes in physicochemical composition in comparison to CS and NC; statistically significant differences were observed only in calcium concentration. |
Cicho’nska et al., 2022 Poland [81] Oral microbioma | Buccal oral mucosa from ECS, CS, NS | Bacterial survival and growth | Observe if there were any changes in oral bacteria of ECS | ECS caused changes in oral bacteria compared to CS and NS, especially with respect to colonization of potentially pathogenic bacteria. |
Cuadra et al., 2019 USA [82] Cariology | S. gordonii, S. intermedius, S. mitis, S. oralis | Bacterial survival and growth | Impact on survival and growth of OCS Exp: various ECs and CS aerosols | Flavorless EC aerosol (± nicotine) is less detrimental to the survival and growth of OCS than CS. |
Fischman et al., 2020 USA [83] Cariology | S. gordonii, S. intermedius, S. mitis, S. oralis | Planktonic growth curves | Effect on the growth of OCS Exp: flavor and flavorless ECS | Flavored e-liquids are more detrimental to the growth of OCS than flavorless e-liquids. |
Franco et al., 2016 Italy [84] Oral cancer | Cytologic exam from ECS, CS, NS | Oral cancer cytologic exam—scraping oral mucosa | Evaluate the safety of EC and to establish their role in the prevention of oral cancer | The use of ECS seems to be safe for oral cells and should be suggested as an aid to smoking cessation. |
Ganesan et al., 2018 USA [85] Oral microbioma | Subgingival plaque | Biofilm architecture changes | Effects on the subgingival microbiome Exp: ECS | The study questions the safety of EC. |
Guo et al., 2021 USA [86] Oral cancer | Buccal human cells | DNA damage | Evaluate the formation of apurinic/apyrimidinic (AP) sites EXP: ECS, CS, NS | Propylene glycol may inhibit bacteria in oral cells, resulting in reduced inflammation and related effects, and reduced AP site levels in ECS DNA. |
Ji et al., 2019 USA [87] Other | Human oral keratinocytes | Gene changes | Impacts on the gene pathways of normal human oral keratinocytes Exp: ECS | EC aerosols upregulate the UPR pathway genes in human oral keratinocytes, as well as the induction of UPR response. |
Kim et al., 2018 USA [88] Cariology | S. mutans | Microbial adhesion to enamel | Cariogenic potential Exp: EC aerosols with sweet flavors | Flavored EC products negatively affect teeth and pose a potential OH risk (similar properties of gelatinous sweets or acidic drinks). |
Kamal et al., 2022 Egypt [89] Oral cancer | Saliva | IL, biomarkers | Evaluate the effect of vaping and cigarette smoking on IL and salivary growth factor compared to NS Exp: ECS, CS, NS | ECS have higher levels of inflammatory and cancer risk biomarkers than NS, but lower than CS. |
Manyaga et al., 2021 USA [90] Oral cancer | Oral cancer cells | Cell viability | Effects on cisplatin resistance in head and neck cancer cells Exp: ECS | EC use might increase chemotherapy resistance. |
Mokeem et al., 2018 Saudi Arabia [91] Oral Candida | Oral rinse from CS, ECS, waterpipe smokers, NS | Oral candida carriage from oral rinse culture | To compare oral Candida carriage among CS, ECS, waterpipe smokers, NS | Oral C. albicans carriage was significantly higher among smokers than NS. |
Nelson et al., 2019 USA [92] Cariology | S. gordonii, S. mitis, S. oralis | Planktonic growth curves | Impact on growth of OCS Exp: ECS and CS | CS is more detrimental to the growth and biofilm formation of OCS than the use of flavorless EC aerosols or liquid ± nicotine. |
Park et al., 2023 USA [93] Oral Microbioma | Sub-gengival plaque and saliva | Bacterial composition/diversity | Evaluate the microbiome and gingival inflammation Exp: ECS, NS | ECS can increase microbial dysbiosis that may lead to periodontal disease. |
Rouabhia et al., 2020 Canada [94] Cariology | S. mutans | Bacterial growth and expression virulence genes | The effect on the growth of S. mutans, the formation of biofilm, and the expression of virulence genes Exp: ECS | EC increased the growth of S. mutans and the expression of virulent genes and promoted the adhesion and formation of biofilms on teeth surfaces. |
Rouabhia et al., 2016 Canada [95] Periodontology | Human gingival ephitelial cells | Cell modification and apoptotic activity | Effects on human gingival epithelial cells Exp: ECS | Exposure to e-cigarette vapor induced cell shape modification and increased LDH activity and mediated cell activity by promoting apoptosis (caspase-3). |
Sancilio et al., 2016 Italy [96] Periodontology | HGF | HGF and ROS production | Effects on HGF Exp: ECS | There is a role for EC fluids in the pathogenesis of oral diseases, such as periodontitis. |
Sancilio et al., 2017 Italy [97] Periodontology | HGF | HGF citotoxicity markers | Effects on HGF Exp: EC liquids (with and without nicotine) | EC liquids (with and without nicotine) trigger molecular and morphologic responses in oral fibroblasts. |
Schwarzmeier et al., 2021 Brasil [98] Other | Exfoliative cytology of the tongue and the mouth from ECS, CS, NS, FS | Oral cells anomalies | To investigate cytogenetic and cytotoxic damage through the evaluation of micronuclei in the oral mucosa of ECS | The use of ECS and alcohol by former smokers can cause more damage to the cells of the oral mucosa compared to those who have not used ECS. |
Shaikh et al., 2019 UK [99] Periodontology | Human gengival mucosa | Cell morphology alterations, healing process | Effects on the proliferation of normal and cancerous monolayer of human oral mucosa and oral wound healing Exp: EC liquid after short-term and medium-term exposure | Medium-term exposure to high concentrations of the EC liquid had cytotoxic effects on normal human oral fibroblasts and keratinocytes. The exposure prolonged the wound healing of NOF and OKF6 oral mucosa cells. |
Sundar et al., 2016 USA [100] Periodontology | Human periodontal fibroblast | ROS presence | Mechanism of gingival epithelial inflammation and pro-senescence in human oral epithelial cells and periodontal ligament fibroblasts Exp: EC aerosols with flavorings | There is a pathologic role of EC aerosol and its flavoring to cells and tissues of the oral cavity. |
Thomas et al., 2022 USA [101] Oral Microbioma | Subgengival plaque | Bacterial composition/diversity | Evaluate the microbiome in subjects with mild periodontitis Exp: ECS, CS, NS | ECS have a unique microbiome that seems healthier than CS, but not compared with NS. |
Tishchenko et al., 2022 Ukraine [102] Oral Microbioma | Plaque from cervical region | Bacterial growth | Evaluate the changes of dental microbiocenosis among adolescents who use devices for heating tobacco products and vaping | ECS promotes opportunistic transient streptococci, while hindering resident plaque microflora. |
Tommasi et al., 2019 USA [103] Oral cancer | Oral ephitelium | Gene transcript deregulation | Regulation of genes and associated molecular pathways, genome-wide, in oral cells Exp: ECS, CS, NS | There is a deregulation of critically important genes and associated molecular pathways in the oral epithelium of vapers that bears both resemblances and differences with that of smokers. |
Tsai et al., 2020 USA [104] Oral cancer | Gingival and tongue squamous cell | Cell invasion and gene expression | impact on gingival squamous cell carcinoma invasion, RAGE expression, and the elaboration of pro-inflammatory molecules. Exp: ECS with flavor and nicotine | Electronic cigarette flavoring and nicotine orchestrate the differential regulation of oral squamous cell carcinoma (OSCC) cell invasion and inflammatory effects. |
Vermehren et al., 2020 Germany [105] Periodontology | HGF | Metabolic activity of HGF | Compare the effects on HGF in terms of proliferation, metabolic activity, cell death, and formation of ROS. Exp: ECS and CS | Exposure of HGF to ECS does not seem to be as harmful as traditional CS. |
Willershausen et al., 2014 Germany [106] Periodontology | HF | HFs proliferation | Influence on the viability and proliferation of human periodontal ligament fibroblasts Exp: different EC liquids | The proliferation rates of the cells incubated with nicotine or the various flavored liquids were reduced in comparison to those of the untreated control cells (not all reductions were statistically significant). |
Zhao et al., 2019 USA [107] Other | Human premolars | Tooth discoloration | Effects on the color of enamel, dentin, and composite resin restorations, as well as the effects of whitening treatments Exp: ECS, CS, red wine, coffee, and soy sauce | Tooth discoloration associated with EC aerosol is minimal. |
Morishita et al., 2022 Japan [108] Oral cancer | Oral mucosal cells | Gene mutations | Regulation of genes and associated molecular pathways, genome-wide, in oral cells Exp: HTP, CS | Heated tobacco products and CS had similar cytotoxic effects. |
Uehara et al., 2023 Japan [109] Oral cancer | Human gingival cells | Gene deregulation | Gene mutation in human cells Exp: heated tobacco products, non- heated tobacco products | Long-term HTP stimulation affected the epithelial differentiation and keratinization of gingival epithelial cells. |
Pagano et al., 2021 Italy [110] Other | HGF and keratinocytes | Cells alterations/biological effects | Effect on cell viability, morphology, migration, apoptosis, and cell cycle Exp: heated tobacco products | HTP extracts increased both cell viability and migration. No morphological alterations were observed. HTP may have clinical effects on oral cell populations. |
Marinucci et al., 2022 Italy [111] Other | HGF and keratinocytes | Cells alterations/biological effects | Effect on cell viability, morphology, migration, apoptosis, cell cycle, and epithelial–mesenchymal transition Exp: heated tobacco products, CS, and EC | CS induced significant damage, EC did not result in morphological and functional alterations in vitro, and HTP mainly modified oral cell function. |
3. Results
3.1. Search
3.2. Observational Studies
3.2.1. Data Synthesis
3.2.2. Risk of Bias across Studies
3.2.3. Main Results of Included Studies
3.2.4. Meta-Analysis
3.3. Interventional Studies
3.3.1. Data Synthesis
3.3.2. Risk of Bias across Studies
3.3.3. Main Results of Included Studies
3.4. Laboratory Studies
3.4.1. Data Synthesis
3.4.2. Risk of Bias across Studies
3.4.3. Main Results of the Included Studies
3.4.4. Meta-Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
Abbreviations
Acronyms | Terms |
ENDS | electronic nicotine delivery systems |
ECS | electronic cigarette smokers |
HTP | heated tobacco products |
CS | cigarettes smokers |
NS | non-smokers |
DS | dual smokers |
OS | other smokers (waterpipe, shisha, etc.) |
FS | former smokers |
References
- McAlinden, K.D.; Eapen, M.S.; Lu, W.; Sharma, P.; Sohal, S.S. The rise of electronic nicotine delivery systems and the emergence of electronic-cigarette-driven disease. Am. J. Physiol. Lung Cell Mol. Physiol. 2020, 319, L585–L595. [Google Scholar] [CrossRef]
- Orellana-Barrios, M.A.; Payne, D.; Mulkey, Z.; Nugent, K. Electronic Cigarettes-A Narrative Review for Clinicians. Am. J. Med. 2015, 128, 674–681. [Google Scholar] [CrossRef] [PubMed]
- Becker, T.D.; Rice, T.R. Youth vaping: A review and update on global epidemiology, physical and behavioral health risks, and clinical considerations. Eur. J. Pediatr. 2021, 181, 453–462. [Google Scholar] [CrossRef] [PubMed]
- Ralho, A.; Coelho, A.; Ribeiro, M.; Paula, A.; Amaro, I.; Sousa, J.; Marto, C.; Ferreira, M.; Carrilho, E. Effects of Electronic Cigarettes on Oral Cavity: A Systematic Review. J. Evid. Based Dent. Pract. 2019, 19, 101318. [Google Scholar] [CrossRef] [PubMed]
- Rom, O.; Pecorelli, A.; Valacchi, G.; Reznick, A.Z. Are E-cigarettes a safe and good alternative to cigarette smoking? Ann. N. Y Acad. Sci. 2015, 1340, 65–74. [Google Scholar] [CrossRef]
- Holliday, R.; Chaffee, B.W.; Jakubovics, N.S.; Kist, R.; Preshaw, P.M. Electronic Cigarettes and Oral Health. J. Dent. Res. 2021, 100, 906–913. [Google Scholar] [CrossRef] [PubMed]
- Ma, S.; Qiu, Z.; Chen, J.; Shang, C. Synthetic nicotine e-liquids sold in US online vape shops. Prev. Med. Rep. 2023, 33, 102222. [Google Scholar] [CrossRef]
- Gaur, S.; Agnihotri, R. Health Effects of Trace Metals in Electronic Cigarette Aerosols—A Systematic Review. Biol. Trace Elem. Res. 2019, 188, 295–315. [Google Scholar] [CrossRef]
- Sood, A.K.; Kesic, M.J.; Hernandez, M.L. Electronic cigarettes: One size does not fit all. J. Allergy Clin. Immunol. 2018, 141, 1973–1982. [Google Scholar] [CrossRef]
- Arora, N.; Dreze, X.; Ghose, A.; Hess, J.D.; Iyengar, R.; Jing, B.; Joshi, Y.; Kumar, V.; Lurie, N.; Neslin, S.; et al. Putting one-to-one marketing to work: Personalization, customization, and choice. Mark. Lett. 2008, 19, 305–321. [Google Scholar] [CrossRef]
- Amato, L.; Cruciani, F.; Solimini, R.; Barca, A.; Pacifici, R.; Davoli, M. Effects of electronic cigarettes on health: A systematic review of the available evidence. Recenti Prog. Med. 2020, 111, 30–43. [Google Scholar] [CrossRef]
- Tattan-Birch, H.; Hartmann-Boyce, J.; Kock, L.; Simonavicius, E.; Brose, L.; Jackson, S.; Shahab, L.; Brown, J. Heated tobacco products for smoking cessation and reducing smoking prevalence. Cochrane Database Syst. Rev. 2022, 1, CD013790. [Google Scholar] [CrossRef] [PubMed]
- Bravo-Gutierrez, O.A.; Falfan-Valencia, R.; Ramirez-Venegas, A.; Sansores, R.H.; Ponciano-Rodriguez, G.; Perez-Rubio, G. Lung Damage Caused by Heated Tobacco Products and Electronic Nicotine Delivery Systems: A Systematic Review. Int. J. Environ. Res. Public Health 2021, 18, 4079. [Google Scholar] [CrossRef] [PubMed]
- Znyk, M.; Jurewicz, J.; Kaleta, D. Exposure to Heated Tobacco Products and Adverse Health Effects, a Systematic Review. Int. J. Environ. Res. Public Health 2021, 18, 6651. [Google Scholar] [CrossRef] [PubMed]
- Kanai, M.; Kanai, O.; Tabuchi, T.; Mio, T. Association of heated tobacco product use with tobacco use cessation in a Japanese workplace: A prospective study. Thorax 2021, 76, 615–617. [Google Scholar] [CrossRef] [PubMed]
- WHO; FDI. Tobacco or Oral Health An Advocacy Guide for Oral Health Professionals; WHO: Geneva, Switzerland, 2005. [Google Scholar]
- Figueredo, C.A.; Abdelhay, N.; Figueredo, C.M.; Catunda, R.; Gibson, M.P. The impact of vaping on periodontitis: A systematic review. Clin. Exp. Dent. Res. 2021, 7, 376–384. [Google Scholar] [CrossRef] [PubMed]
- Graves, D.T.; Li, J.; Cochran, D.L. Inflammation and uncoupling as mechanisms of periodontal bone loss. J. Dent. Res. 2011, 90, 143–153. [Google Scholar] [CrossRef] [PubMed]
- Baltacioglu, E.; Akalin, F.A.; Alver, A.; Deger, O.; Karabulut, E. Protein carbonyl levels in serum and gingival crevicular fluid in patients with chronic periodontitis. Arch. Oral Biol. 2008, 53, 716–722. [Google Scholar] [CrossRef]
- Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021, 372, n71. [Google Scholar] [CrossRef]
- Muka, T.; Glisic, M.; Milic, J.; Verhoog, S.; Bohlius, J.; Bramer, W.; Chowdhury, R.; Franco, O.H. A 24-step guide on how to design, conduct, and successfully publish a systematic review and meta-analysis in medical research. Eur. J. Epidemiol. 2020, 35, 49–60. [Google Scholar] [CrossRef]
- Lindemann, E.A.; Chen, E.S.; Wang, Y.; Skube, S.J.; Melton, G.B. Representation of Social History Factors Across Age Groups: A Topic Analysis of Free-Text Social Documentation. AMIA Annu. Symp. Proc. 2017, 2017, 1169–1178. [Google Scholar] [PubMed]
- Sterne, J.A.C.; Savovic, J.; Page, M.J.; Elbers, R.G.; Blencowe, N.S.; Boutron, I.; Cates, C.J.; Cheng, H.Y.; Corbett, M.S.; Eldridge, S.M.; et al. RoB 2: A revised tool for assessing risk of bias in randomised trials. BMJ 2019, 366, l4898. [Google Scholar] [CrossRef] [PubMed]
- Sterne, J.A.; Hernan, M.A.; Reeves, B.C.; Savovic, J.; Berkman, N.D.; Viswanathan, M.; Henry, D.; Altman, D.G.; Ansari, M.T.; Boutron, I.; et al. ROBINS-I: A tool for assessing risk of bias in non-randomised studies of interventions. BMJ 2016, 355, i4919. [Google Scholar] [CrossRef] [PubMed]
- Rooney, A.A.; Boyles, A.L.; Wolfe, M.S.; Bucher, J.R.; Thayer, K.A. Systematic review and evidence integration for literature-based environmental health science assessments. Environ. Health Perspect. 2014, 122, 711–718. [Google Scholar] [CrossRef] [PubMed]
- Higgins, J.P.; Thompson, S.G. Quantifying heterogeneity in a meta-analysis. Stat. Med. 2002, 21, 1539–1558. [Google Scholar] [CrossRef] [PubMed]
- Higgins, J.P.; Altman, D.G.; Gotzsche, P.C.; Juni, P.; Moher, D.; Oxman, A.D.; Savovic, J.; Schulz, K.F.; Weeks, L.; Sterne, J.A.; et al. The Cochrane Collaboration’s tool for assessing risk of bias in randomised trials. BMJ 2011, 343, d5928. [Google Scholar] [CrossRef] [PubMed]
- Al-Aali, K.A.; Alrabiah, M.; ArRejaie, A.S.; Abduljabbar, T.; Vohra, F.; Akram, Z. Peri-implant parameters, tumor necrosis factor-alpha, and interleukin-1 beta levels in vaping individuals. Clin. Implant. Dent. Relat. Res. 2018, 20, 410–415. [Google Scholar] [CrossRef] [PubMed]
- Alazmi, S.O.; Almutairi, F.J.; Alresheedi, B.A. Comparison of Peri-Implant Clinicoradiographic Parameters among Non-Smokers and Individuals Using Electronic Nicotine Delivery Systems at 8 Years of Follow-up. Oral Health Prev. Dent. 2021, 19, 511–516. [Google Scholar] [CrossRef]
- Ali, D.; Kuyunov, I.; Baskaradoss, J.K.; Mikami, T. Comparison of periodontal status and salivary IL-15 and -18 levels in cigarette-smokers and individuals using electronic nicotine delivery systems. BMC Oral Health 2022, 22, 655. [Google Scholar] [CrossRef]
- AlQahtani, M.A.; Alayad, A.S.; Alshihri, A.; Correa, F.O.B.; Akram, Z. Clinical peri-implant parameters and inflammatory cytokine profile among smokers of cigarette, e-cigarette, and waterpipe. Clin. Implant. Dent. Relat. Res. 2018, 20, 1016–1021. [Google Scholar] [CrossRef]
- Alqahtani, F.; Alqahtani, M.; Albaqawi, A.H.; Al-Kheraif, A.A.; Javed, F. Comparison of cotinine levels in the peri-implant sulcular fluid among cigarette and waterpipe smokers, electronic-cigarette users, and nonsmokers. Clin. Implant. Dent. Relat. Res. 2019, 21, 702–707. [Google Scholar] [CrossRef]
- Alqahtani, A.S.; Alqhtani, N.R.; Gufran, K.; Alsakr, A.M.; Alshehri, A.; Binaljadm, T.M.; Alzamil, F.F.; Alqwiri, A.S.; Alotaibi, N.M.; Harun, H.M.W. Comparative assessment of periodontal treatment needs among the electronic cigarette users and traditional smokers. Eur. Rev. Med. Pharmacol. Sci. 2022, 26, 2676–2682. [Google Scholar] [CrossRef]
- ArRejaie, A.S.; Al-Aali, K.A.; Alrabiah, M.; Vohra, F.; Mokeem, S.A.; Basunbul, G.; Alrahlah, A.; Abduljabbar, T. Proinflammatory cytokine levels and peri-implant parameters among cigarette smokers, individuals vaping electronic cigarettes, and non-smokers. J. Periodontol. 2019, 90, 367–374. [Google Scholar] [CrossRef] [PubMed]
- Bardellini, E.; Amadori, F.; Conti, G.; Majorana, A. Oral mucosal lesions in electronic cigarettes consumers versus former smokers. Acta Odontol. Scand. 2018, 76, 226–228. [Google Scholar] [CrossRef]
- BinShabaib, M.; Alharthi, S.S.; Akram, Z.; Khan, J.; Rahman, I.; Romanos, G.E.; Javed, F. Clinical periodontal status and gingival crevicular fluid cytokine profile among cigarette-smokers, electronic-cigarette users and never-smokers. Arch. Oral Biol. 2019, 102, 212–217. [Google Scholar] [CrossRef] [PubMed]
- Dalrymple, A.; Coburn, S.; Brandt, M.; Hardie, G.; Murphy, J. Pilot study to determine differences in breath odour between cigarette and e-cigarette consumers. Sci. Rep. 2022, 12, 2204. [Google Scholar] [CrossRef] [PubMed]
- Ghazali, A.I.A.; Ismail, A.F.; Daud, A. Caries Experience among Cigarette and E-Cigarette Users: A 6-Month Prospective Study. J. Pharm. Sci. Res. 2019, 11, 2566–2569. [Google Scholar]
- Herndon, P.; Jassal, J.S.; Cramer, J.D. Association between E-cigarette use and oral HPV-16 infection. Oral Oncol. 2022, 125, 105676. [Google Scholar] [CrossRef] [PubMed]
- Ibraheem, W.I.; Fageeh, H.I.; Preethanath, R.S.; Alzahrani, F.A.; Al-Zawawi, A.S.; Divakar, D.D.; Al-Kheraif, A.A. Comparison of RANKL and osteoprotegerin levels in the gingival crevicular fluid of young cigarette- and waterpipe-smokers and individuals using electronic nicotine delivery systems. Arch. Oral Biol. 2020, 115, 104714. [Google Scholar] [CrossRef] [PubMed]
- Javed, F.; Abduljabbar, T.; Vohra, F.; Malmstrom, H.; Rahman, I.; Romanos, G.E. Comparison of Periodontal Parameters and Self-Perceived Oral Symptoms Among Cigarette Smokers, Individuals Vaping Electronic Cigarettes, and Never-Smokers. J. Periodontol. 2017, 88, 1059–1065. [Google Scholar] [CrossRef]
- Jeong, W.; Choi, D.W.; Kim, Y.K.; Lee, H.J.; Lee, S.A.; Park, E.C.; Jang, S.I. Associations of electronic and conventional cigarette use with periodontal disease in South Korean adults. J. Periodontol. 2020, 91, 55–64. [Google Scholar] [CrossRef]
- Karaaslan, F.; Dikilitaş, A.; Yiğit, U. The effects of vaping electronic cigarettes on periodontitis. Aust. Dent. J. 2020, 65, 143–149. [Google Scholar] [CrossRef] [PubMed]
- Mokeem, S.A.; Alasqah, M.N.; Michelogiannakis, D.; Al-Kheraif, A.A.; Romanos, G.E.; Javed, F. Clinical and radiographic periodontal status and whole salivary cotinine, IL-1β and IL-6 levels in cigarette- and waterpipe-smokers and E-cig users. Environ. Toxicol. Pharmacol. 2018, 61, 38–43. [Google Scholar] [CrossRef]
- Tatullo, M.; Gentile, S.; Paduano, F.; Santacroce, L.; Marrelli, M. Crosstalk between oral and general health status in e-smokers. Medicine 2016, 95, e5589. Available online: https://journals.lww.com/00005792-201612060-201600074 (accessed on 17 August 2023). [CrossRef] [PubMed]
- Vohra, F.; Bukhari, I.A.; Sheikh, S.A.; Albaijan, R.; Naseem, M. Comparison of self-rated oral symptoms and periodontal status among cigarette smokers and individuals using electronic nicotine delivery systems. J. Am. Coll. Health 2020, 68, 788–793. [Google Scholar] [CrossRef]
- Akinkugbe, A.A. Cigarettes, E-cigarettes, and Adolescents’ Oral Health: Findings from the Population Assessment of Tobacco and Health (PATH) Study. JDR Clin. Trans. Res. 2019, 4, 276–283. [Google Scholar] [CrossRef] [PubMed]
- Alade, O.; Folayan, M.O.; Adeniyi, A.; Adeyemo, Y.I.; Oyapero, A.; Olatosi, O.O.; Nzomiwu, C.; Popoola, B.O.; Eigbobo, J.; Oziegbe, E.; et al. Differences in Oral Lesions Associated with Tobacco Smoking, E-Cigarette Use and COVID-19 Infection among Adolescents and Young People in Nigeria. Int. J. Environ. Res. Public Health 2022, 19, 10509. [Google Scholar] [CrossRef]
- Alhajj, M.N.; Al-Maweri, S.A.; Folayan, M.O.; Halboub, E.; Khader, Y.; Omar, R.; Amran, A.G.; Al-Batayneh, O.B.; Celebić, A.; Persic, S.; et al. Oral health practices and self-reported adverse effects of E-cigarette use among dental students in 11 countries: An online survey. BMC Oral Health 2022, 22, 18. [Google Scholar] [CrossRef]
- AlQobaly, L.; Abed, H.; Alsahafi, Y.; Sabbah, W.; Hakeem, F.F. Does smoking explain the association between use of e-cigarettes and self-reported periodontal disease? J. Dent. 2022, 122, 104164. [Google Scholar] [CrossRef]
- Atuegwu, N.; Perez, M.; Oncken, C.; Thacker, S.; Mead, E.; Mortensen, E. Association between Regular Electronic Nicotine Product Use and Self-Reported Periodontal Disease Status: Population Assessment of Tobacco and Health Survey. Int. J. Environ. Res. Public Health 2019, 16, 1263. [Google Scholar] [CrossRef]
- Cho, J.H. The association between electronic-cigarette use and self-reported oral symptoms including cracked or broken teeth and tongue and/or inside-cheek pain among adolescents: A cross-sectional study. PLoS ONE 2017, 12, e0180506. [Google Scholar] [CrossRef] [PubMed]
- Huilgol, P.; Bhatt, S.P.; Biligowda, N.; Wright, N.C.; Wells, J.M. Association of e-cigarette use with oral health: A population-based cross-sectional questionnaire study. J. Public Health 2019, 41, 354–361. [Google Scholar] [CrossRef] [PubMed]
- Irusa, K.F.; Finkelman, M.; Magnuson, B.; Donovan, T.; Eisen, S.E. A comparison of the caries risk between patients who use vapes or electronic cigarettes and those who do not: A cross-sectional study. J. Am. Dent. Assoc. 2022, 153, 1179–1183. [Google Scholar] [CrossRef]
- Abafalvi, L.; Penzes, M.; Urban, R.; Foley, K.L.; Kaan, R.; Kispelyi, B.; Hermann, P. Perceived health effects of vaping among Hungarian adult e-cigarette-only and dual users: A cross-sectional internet survey. BMC Public Health 2019, 19, 302. [Google Scholar] [CrossRef] [PubMed]
- Vemulapalli, A.; Mandapati, S.R.; Kotha, A.; Aryal, S. Association between vaping and untreated caries. J. Am. Dent. Assoc. 2021, 152, 720–729. [Google Scholar] [CrossRef]
- Vora, M.V.; Chaffee, B.W. Tobacco-use patterns and self-reported oral health outcomes. J. Am. Dent. Assoc. 2019, 150, 332–344.e2. [Google Scholar] [CrossRef] [PubMed]
- Yoshioka, T.; Tabuchi, T. Combustible cigarettes, heated tobacco products, combined product use, and periodontal disease: A cross-sectional JASTIS study. PLoS ONE 2021, 16, e0248989. [Google Scholar] [CrossRef] [PubMed]
- Akram, Z.; Aati, S.; Alrahlah, A.; Vohra, F.; Fawzy, A. Longitudinal evaluation of clinical, spectral and tissue degradation biomarkers in progression of periodontitis among cigarette and electronic cigarette smokers. J. Dent. 2021, 109, 103678. [Google Scholar] [CrossRef]
- Al Deeb, M.; Alresayes, S.; A Mokeem, S.; Alhenaki, A.M.; AlHelal, A.; Shafqat, S.S.; Vohra, F.; Abduljabbar, T. Clinical and immunological peri-implant parameters among cigarette and electronic smoking patients treated with photochemotherapy: A randomized controlled clinical trial. Photodiagn. Photodyn. Ther. 2020, 31, 101800. [Google Scholar] [CrossRef]
- Al-Hamoudi, N.; Alsahhaf, A.; Al Deeb, M.; Alrabiah, M.; Vohra, F.; Abduljabbar, T. Effect of scaling and root planing on the expression of anti-inflammatory cytokines (IL-4, IL-9, IL-10, and IL-13) in the gingival crevicular fluid of electronic cigarette users and non-smokers with moderate chronic periodontitis. J. Periodontal Implant. Sci. 2020, 50, 74. [Google Scholar] [CrossRef]
- Alharthi, S.S.; BinShabaib, M.; Akram, Z.; Rahman, I.; Romanos, G.E.; Javed, F. Impact of cigarette smoking and vaping on the outcome of full-mouth ultrasonic scaling among patients with gingival inflammation: A prospective study. Clin. Oral Investig. 2019, 23, 2751–2758. [Google Scholar] [CrossRef]
- Alhumaidan, A.A.; Al-Aali, K.A.; Vohra, F.; Javed, F.; Abduljabbar, T. Comparison of Whole Salivary Cortisol and Interleukin 1-Beta Levels in Light Cigarette-Smokers and Users of Electronic Nicotine Delivery Systems before and after Non-Surgical Periodontal Therapy. Int. J. Environ. Res. Public Health 2022, 19, 11290. [Google Scholar] [CrossRef] [PubMed]
- AlJasser, R.; Zahid, M.; AlSarhan, M.; AlOtaibi, D.; AlOraini, S. The effect of conventional versus electronic cigarette use on treatment outcomes of peri-implant disease. BMC Oral Health 2021, 21, 480. [Google Scholar] [CrossRef]
- Al Rifaiy, M.Q.; Qutub, O.A.; Alasqah, M.N.; Al-Sowygh, Z.H.; Mokeem, S.A.; Alrahlah, A. Effectiveness of adjunctive antimicrobial photodynamic therapy in reducing peri-implant inflammatory response in individuals vaping electronic cigarettes: A randomized controlled clinical trial. Photodiagn. Photodyn. Ther. 2018, 22, 132–136. Available online: https://linkinghub.elsevier.com/retrieve/pii/S1572100018300711 (accessed on 17 August 2023). [CrossRef]
- Alshibani, N.; Alssum, L.; Basudan, A.; Shaheen, M.; Alqutub, M.N.; Dahash, F.A.; Alkattan, R. Non-surgical periodontal therapy with adjunct photodynamic therapy for the management of periodontal inflammation in adults using nicotine-free electronic-cigarette: A randomized control trial. Photodiagn. Photodyn. Ther. 2022, 38, 102820. [Google Scholar] [CrossRef]
- Reuther, W.J.; Hale, B.; Matharu, J.; Blythe, J.N.; Brennan, P.A. Do you mind if I vape? Immediate effects of electronic cigarettes on perfusion in buccal mucosal tissue—A pilot study. Br. J. Oral Maxillofac. Surg. 2016, 54, 338–341. [Google Scholar] [CrossRef]
- Wadia, R.; Booth, V.; Yap, H.F.; Moyes, D.L. A pilot study of the gingival response when smokers switch from smoking to vaping. Br. Dent. J. 2016, 221, 722–726. [Google Scholar] [CrossRef]
- Xu, F.; Pushalkar, S.; Lin, Z.; Thomas, S.C.; Persaud, J.K.; Sierra, M.A.; Vardhan, M.; Vasconcelos, R.; Akapo, A.; Guo, Y.; et al. Electronic cigarette use enriches periodontal pathogens. Mol. Oral Microbiol. 2022, 37, 63–76. [Google Scholar] [CrossRef] [PubMed]
- Pouly, S.; Ng, W.T.; Blanc, N.; Hession, P.; Zanetti, F.; Battey, J.N.D.; de La Bourdonnaye, G.; Heremans, A.; Haziza, C. Effect of switching from cigarette smoking to the use of the tobacco heating system on periodontitis treatment outcome: Periodontal parameter results from a multicenter Japanese study. Front. Dent. Med. 2022, 3, 915079. [Google Scholar] [CrossRef]
- Alanazi, H.; Semlali, A.; Chmielewski, W.; Rouabhia, M. E-Cigarettes Increase Candida albicans Growth and Modulate its Interaction with Gingival Epithelial Cells. Int. J. Environ. Res. Public Health 2019, 16, 294. [Google Scholar] [CrossRef] [PubMed]
- Alanazi, H.; Park, H.J.; Chakir, J.; Semlali, A.; Rouabhia, M. Comparative study of the effects of cigarette smoke and electronic cigarettes on human gingival fibroblast proliferation, migration and apoptosis. Food Chem. Toxicol. 2018, 118, 390–398. [Google Scholar] [CrossRef] [PubMed]
- Aldakheel, F.M.; Alduraywish, S.A.; Jhugroo, P.; Jhugroo, C.; Divakar, D.D. Quantification of pathogenic bacteria in the subgingival oral biofilm samples collected from cigarette-smokers, individuals using electronic nicotine delivery systems and non-smokers with and without periodontitis. Arch. Oral Biol. 2020, 117, 104793. [Google Scholar] [CrossRef]
- Alzoubi, H.; Abu-Lubad, M.; Al-Mnayyis, A.a.; Satari, A.; Alzobi, M.; Ramadneh, M.A.; Jarajreh, D.a. Effect of Electronic Cigarettes on the Carriage of Selected Organisms in the Nasal and Oral Cavity in Comparison to Tobacco Smokers and Non-smokers. J. Clin. Diagn. Res. 2020, 14, DC11–DC15. Available online: https://jcdr.net/article_fulltext.asp?issn=0973-709x&year=2020&volume=14&issue=7&page=DC11&issn=0973-709x&id=13852 (accessed on 17 August 2023). [CrossRef]
- Catala-Valentin, A.; Bernard, J.N.; Caldwell, M.; Maxson, J.; Moore, S.D.; Andl, C.D. E-Cigarette Aerosol Exposure Favors the Growth and Colonization of Oral Streptococcus mutans Compared to Commensal Streptococci. Microbiol. Spectr. 2022, 10, e0242121. [Google Scholar] [CrossRef]
- Cátala-Valentín, A.R.; Almeda, J.; Bernard, J.N.; Cole, A.M.; Cole, A.L.; Moore, S.D.; Andl, C.D. E-Cigarette Aerosols Promote Oral S. aureus Colonization by Delaying an Immune Response and Bacterial Clearing. Cells 2022, 11, 773. [Google Scholar] [CrossRef] [PubMed]
- Chopyk, J.; Bojanowski, C.M.; Shin, J.; Moshensky, A.; Fuentes, A.L.; Bonde, S.S.; Chuki, D.; Pride, D.T.; Crotty Alexander, L.E. Compositional Differences in the Oral Microbiome of E-cigarette Users. Front. Microbiol. 2021, 12, 599664. [Google Scholar] [CrossRef]
- Cichonska, D.; Kusiak, A.; Kochanska, B.; Ochocinska, J.; Swietlik, D. Influence of Electronic Cigarettes on Selected Antibacterial Properties of Saliva. Int. J. Environ. Res. Public Health 2019, 16, 4433. [Google Scholar] [CrossRef]
- Cichonska, D.; Krol, O.; Slominska, E.M.; Kochanska, B.; Swietlik, D.; Ochocinska, J.; Kusiak, A. Influence of Electronic Cigarettes on Antioxidant Capacity and Nucleotide Metabolites in Saliva. Toxics 2021, 9, 263. [Google Scholar] [CrossRef]
- Cichonska, D.; Kusiak, A.; Kochanska, B.; Ochocinska, J.; Swietlik, D. Influence of Electronic Cigarettes on Selected Physicochemical Properties of Saliva. Int. J. Environ. Res. Public Health 2022, 19, 3314. [Google Scholar] [CrossRef] [PubMed]
- Cichonska, D.; Kusiak, A.; Piechowicz, L.; Swietlik, D. A pilot investigation into the influence of electronic cigarettes on oral bacteria. Postepy Dermatol. Alergol. 2021, 38, 1092–1098. [Google Scholar] [CrossRef]
- Cuadra, G.A.; Smith, M.T.; Nelson, J.M.; Loh, E.K.; Palazzolo, D.L. A Comparison of Flavorless Electronic Cigarette-Generated Aerosol and Conventional Cigarette Smoke on the Survival and Growth of Common Oral Commensal Streptococci. Int. J. Environ. Res. Public Health 2019, 16, 1669. [Google Scholar] [CrossRef] [PubMed]
- Fischman, J.S.; Sista, S.; Lee, D.; Cuadra, G.A.; Palazzolo, D.L. Flavorless vs. Flavored Electronic Cigarette-Generated Aerosol and E-Liquid on the Growth of Common Oral Commensal Streptococci. Front. Physiol. 2020, 11, 585416. [Google Scholar] [CrossRef]
- Franco, T.; Trapasso, S.; Puzzo, L.; Allegra, E. Electronic Cigarette: Role in the Primary Prevention of Oral Cavity Cancer. Clin. Med. Insights Ear Nose Throat 2016, 9, 7–12. [Google Scholar] [CrossRef] [PubMed]
- Ganesan, S.M.; Dabdoub, S.M.; Nagaraja, H.N.; Scott, M.L.; Pamulapati, S.; Berman, M.L.; Shields, P.G.; Wewers, M.E.; Kumar, P.S. Adverse effects of electronic cigarettes on the disease-naive oral microbiome. Sci. Adv. 2020, 6, eaaz0108. [Google Scholar] [CrossRef] [PubMed]
- Guo, J.; Hecht, S.S. DNA damage in human oral cells induced by use of e-cigarettes. Drug Test. Anal. 2022, in press. [Google Scholar] [CrossRef]
- Ji, E.H.; Elzakra, N.; Chen, W.; Cui, L.; Lee, E.S.; Sun, B.; Messadi, D.; Xia, T.; Zhu, Y.; Hu, S. E-cigarette aerosols induce unfolded protein response in normal human oral keratinocytes. J. Cancer 2019, 10, 6915–6924. [Google Scholar] [CrossRef] [PubMed]
- Kim, S.A.; Smith, S.; Beauchamp, C.; Song, Y.; Chiang, M.; Giuseppetti, A.; Frukhtbeyn, S.; Shaffer, I.; Wilhide, J.; Routkevitch, D.; et al. Cariogenic potential of sweet flavors in electronic-cigarette liquids. PLoS ONE 2018, 13, e0203717. [Google Scholar] [CrossRef]
- Kamal, N.M.; Shams, N.S. The impact of tobacco smoking and electronic cigarette vaping on salivary biomarkers. A comparative study. Saudi Dent. J. 2022, 34, 404–409. [Google Scholar] [CrossRef]
- Manyanga, J.; Ganapathy, V.; Bouharati, C.; Mehta, T.; Sadhasivam, B.; Acharya, P.; Zhao, D.; Queimado, L. Electronic cigarette aerosols alter the expression of cisplatin transporters and increase drug resistance in oral cancer cells. Sci. Rep. 2021, 11, 1821. [Google Scholar] [CrossRef]
- Mokeem, S.A.; Abduljabbar, T.; Al-Kheraif, A.A.; Alasqah, M.N.; Michelogiannakis, D.; Samaranayake, L.P.; Javed, F. Oral Candida carriage among cigarette- and waterpipe-smokers, and electronic cigarette users. Oral Dis. 2019, 25, 319–326. [Google Scholar] [CrossRef]
- Nelson, J.M.; Cuadra, G.A.; Palazzolo, D.L. A Comparison of Flavorless Electronic Cigarette-Generated Aerosol and Conventional Cigarette Smoke on the Planktonic Growth of Common Oral Commensal Streptococci. Int. J. Environ. Res. Public Health 2019, 16, 5004. [Google Scholar] [CrossRef] [PubMed]
- Park, B.; Koh, H.; Patatanian, M.; Reyes-Caballero, H.; Zhao, N.; Meinert, J.; Holbrook, J.T.; Leinbach, L.I.; Biswal, S. The mediating roles of the oral microbiome in saliva and subgingival sites between e-cigarette smoking and gingival inflammation. BMC Microbiol. 2023, 23, 35. [Google Scholar] [CrossRef]
- Rouabhia, M.; Semlali, A. Electronic cigarette vapor increases Streptococcus mutans growth, adhesion, biofilm formation, and expression of the biofilm-associated genes. Oral Dis. 2021, 27, 639–647. [Google Scholar] [CrossRef] [PubMed]
- Rouabhia, M.; Park, H.J.; Semlali, A.; Zakrzewski, A.; Chmielewski, W.; Chakir, J. E-Cigarette Vapor Induces an Apoptotic Response in Human Gingival Epithelial Cells Through the Caspase-3 Pathway: Effect of E-Cigarette on Epithelial Cells. J. Cell. Physiol. 2017, 232, 1539–1547. [Google Scholar] [CrossRef]
- Sancilio, S.; Gallorini, M.; Cataldi, A.; di Giacomo, V. Cytotoxicity and apoptosis induction by e-cigarette fluids in human gingival fibroblasts. Clin. Oral Investig. 2016, 20, 477–483. Available online: http://link.springer.com/410.1007/s00784-00015-01537-x (accessed on 17 August 2023). [CrossRef] [PubMed]
- Sancilio, S.; Gallorini, M.; Cataldi, A.; Sancillo, L.; Rana, R.A.; di Giacomo, V. Modifications in Human Oral Fibroblast Ultrastructure, Collagen Production, and Lysosomal Compartment in Response to Electronic Cigarette Fluids. J. Periodontol. 2017, 88, 673–680. [Google Scholar] [CrossRef] [PubMed]
- Schwarzmeier, L.A.T.; da Cruz, B.S.; Ferreira, C.C.P.; Carvalho, B.; Alves, M.G.O.; Lima Carta, C.F.; Scholz, J.R.; Almeida, J.D. E-cig might cause cell damage of oral mucosa. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 2021, 131, 435–443. [Google Scholar] [CrossRef]
- Shaikh, Z.N.; Alqahtani, A.; Almela, T.; Franklin, K.; Tayebi, L.; Moharamzadeh, K. Effects of electronic cigarette liquid on monolayer and 3D tissue-engineered models of human gingival mucosa. J. Adv. Periodontol. Implant. Dent. 2019, 11, 54–62. [Google Scholar] [CrossRef]
- Sundar, I.K.; Javed, F.; Romanos, G.E.; Rahman, I. E-cigarettes and flavorings induce inflammatory and pro-senescence responses in oral epithelial cells and periodontal fibroblasts. Oncotarget 2016, 7, 77196–77204. [Google Scholar] [CrossRef]
- Thomas, S.C.; Xu, F.; Pushalkar, S.; Lin, Z.; Thakor, N.; Vardhan, M.; Flaminio, Z.; Khodadadi-Jamayran, A.; Vasconcelos, R.; Akapo, A.; et al. Electronic Cigarette Use Promotes a Unique Periodontal Microbiome. mBio 2022, 13, e0007522. [Google Scholar] [CrossRef]
- Tishchenko, O.V.; Kryvenko, L.S.; Gargina, V.V. Influence of smoking heating up tobacco products and e-cigarettes on the microbiota of dental plaque. Pol. Merkur. Lekarski 2022, 50, 16–20. [Google Scholar]
- Tommasi, S.; Caliri, A.; Caceres, A.; Moreno, D.; Li, M.; Chen, Y.; Siegmund, K.; Besaratinia, A. Deregulation of Biologically Significant Genes and Associated Molecular Pathways in the Oral Epithelium of Electronic Cigarette Users. Int. J. Mol. Sci. 2019, 20, 738. [Google Scholar] [CrossRef] [PubMed]
- Tsai, K.Y.F.; Hirschi Budge, K.M.; Lepre, A.P.; Rhees, M.S.; Ajdaharian, J.; Geiler, J.; Epperson, D.G.; Astle, K.J.; Winden, D.R.; Arroyo, J.A.; et al. Cell invasion, RAGE expression, and inflammation in oral squamous cell carcinoma (OSCC) cells exposed to e-cigarette flavoring. Clin. Exp. Dent. Res. 2020, 6, 618–625. [Google Scholar] [CrossRef]
- Vermehren, M.F.; Wiesmann, N.; Deschner, J.; Brieger, J.; Al-Nawas, B.; Kämmerer, P.W. Comparative analysis of the impact of e-cigarette vapor and cigarette smoke on human gingival fibroblasts. Toxicol. In Vitro 2020, 69, 105005. [Google Scholar] [CrossRef] [PubMed]
- Willershausen, I.; Wolf, T.; Weyer, V.; Sader, R.; Ghanaati, S.; Willershausen, B. Influence of E-smoking liquids on human periodontal ligament fibroblasts. Head Face Med. 2014, 10, 39. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.; Zanetti, F.; Wang, L.; Pan, J.; Majeed, S.; Malmstrom, H.; Peitsch, M.C.; Hoeng, J.; Ren, Y. Effects of different discoloration challenges and whitening treatments on dental hard tissues and composite resin restorations. J. Dent. 2019, 89, 103182. [Google Scholar] [CrossRef]
- Morishita, Y.; Hasegawa, S.; Koie, S.; Ueda, S.; Miyabe, S.; Watanabe, S.; Goto, M.; Miyachi, H.; Nomoto, S.; Nagao, T. Cytotoxic, genotoxic, and toxicogenomic effects of heated tobacco products and cigarette smoke in human primary keratinocytes. Tob. Induc. Dis. 2022, 20, 82. [Google Scholar] [CrossRef]
- Uehara, O.; Nakamoto, N.; Hiraki, D.; Paudel, D.; Sugiyama, N.; Morikawa, T.; Yoshida, K.; Kawano, Y.; Shimo, T.; Furuichi, Y.; et al. Effects of prolonged stimulation with heated tobacco products (Ploom TECH+) on gingival epithelial cells. J. Periodontal Res. 2023, 58, 553–563. [Google Scholar] [CrossRef] [PubMed]
- Pagano, S.; Negri, P.; Coniglio, M.; Bruscoli, S.; Di Michele, A.; Marchetti, M.C.; Valenti, C.; Gambelunghe, A.; Fanasca, L.; Billi, M.; et al. Heat-not-burn tobacco (IQOS), oral fibroblasts and keratinocytes: Cytotoxicity, morphological analysis, apoptosis and cellular cycle. An in vitro study. J. Periodontal Res. 2021, 56, 917–928. [Google Scholar] [CrossRef]
- Marinucci, L.; Coniglio, M.; Valenti, C.; Massari, S.; Di Michele, A.; Billi, M.; Bruscoli, S.; Negri, P.; Lombardo, G.; Cianetti, S.; et al. In Vitro effects of alternative smoking devices on oral cells: Electronic cigarette and heated tobacco product versus tobacco smoke. Arch. Oral Biol. 2022, 144, 105550. [Google Scholar] [CrossRef]
- Abdul, N.S.; Alshehri, N.M.; Bindawis, H.M.; Alzahrani, H.K.; Alanezi, A.F. Awareness of the Effects of Shisha and Electronic Cigarette Smoking on Oral Health In Saudi Population. Ann. Dent. Spec. 2020, 8, 41. [Google Scholar]
- Kaán, R.; Pénzes, M.; Abafalvi, L.; Hermann, P.; Kispélyi, B. Oral Hygiene Practices of Hungarian Adult E-Cigarette-Only and Dual Users. Oral Health Prev. Dent. 2020, 18, 991–998. [Google Scholar] [CrossRef] [PubMed]
- Isik Andrikopoulos, G.; Farsalinos, K.; Poulas, K. Electronic Nicotine Delivery Systems (ENDS) and Their Relevance in Oral Health. Toxics 2019, 7, 61. [Google Scholar] [CrossRef]
- Ramôa, C.P.; Eissenberg, T.; Sahingur, S.E. Increasing popularity of waterpipe tobacco smoking and electronic cigarette use: Implications for oral healthcare. J. Periodontal Res. 2017, 52, 813–823. [Google Scholar] [CrossRef] [PubMed]
- Laverty, A.A.; Vardavas, C.I.; Filippidis, F.T. Prevalence and reasons for use of Heated Tobacco Products (HTP) in Europe: An analysis of Eurobarometer data in 28 countries. Lancet Reg. Health Eur. 2021, 8, 100159. [Google Scholar] [CrossRef] [PubMed]
- Sultan, A.S.; Jessri, M.; Farah, C.S. Electronic nicotine delivery systems: Oral health implications and oral cancer risk. J. Oral Pathol. Med. 2021, 50, 316–322. [Google Scholar] [CrossRef] [PubMed]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Camoni, N.; Conti, G.; Esteves-Oliveira, M.; Carvalho, T.S.; Roccuzzo, A.; Cagetti, M.G.; Campus, G. Electronic Cigarettes, Heated Tobacco Products, and Oral Health: A Systematic Review and Meta-Analysis. Appl. Sci. 2023, 13, 9654. https://doi.org/10.3390/app13179654
Camoni N, Conti G, Esteves-Oliveira M, Carvalho TS, Roccuzzo A, Cagetti MG, Campus G. Electronic Cigarettes, Heated Tobacco Products, and Oral Health: A Systematic Review and Meta-Analysis. Applied Sciences. 2023; 13(17):9654. https://doi.org/10.3390/app13179654
Chicago/Turabian StyleCamoni, Nicole, Giulio Conti, Marcella Esteves-Oliveira, Thiago Saad Carvalho, Andrea Roccuzzo, Maria Grazia Cagetti, and Guglielmo Campus. 2023. "Electronic Cigarettes, Heated Tobacco Products, and Oral Health: A Systematic Review and Meta-Analysis" Applied Sciences 13, no. 17: 9654. https://doi.org/10.3390/app13179654