Effect of Switching to the Tobacco Heating System Versus Continued Cigarette Smoking on Chronic Generalized Periodontitis Treatment Outcome: Protocol for a Randomized Controlled Multicenter Study

Sandrine Pouly, Wee Teck Ng, Muriel Benzimra, Alexandre Soulan, Nicolas Blanc, Filippo Zanetti, Patrick Picavet, Gizelle Baker, Christelle Haziza, Sandrine Pouly, Wee Teck Ng, Muriel Benzimra, Alexandre Soulan, Nicolas Blanc, Filippo Zanetti, Patrick Picavet, Gizelle Baker, Christelle Haziza

Abstract

Background: Smoking is a significant risk factor for periodontal disease and tooth loss, as shown in several clinical studies comparing smokers and nonsmokers. Although only a few longitudinal studies have assessed the outcome of periodontal disease after smoking cessation, they indicated that recovery after nonsurgical treatment was more successful in those who had quit smoking. As part of tobacco harm reduction strategies, substituting cigarettes with alternative, less harmful tobacco products is an approach complementary to cessation for smokers who would otherwise continue to smoke. The Tobacco Heating System (THS), developed by Philip Morris International (commercialized as IQOS), is part of the heat-not-burn product category. The IQOS device electrically heats tobacco instead of burning it, at much lower temperatures than cigarettes, thereby producing substantially lower levels of harmful and potentially harmful constituents, while providing the nicotine, taste, ritual, and a sensory experience that closely parallel those of cigarettes. Phillip Morris International has published the results from a broad clinical assessment program, which was established to scientifically substantiate the harm reduction potential of the THS among adult healthy smokers switching to the THS. The program is now progressing toward including adult smokers with smoking-related diseases.

Objective: The goal of this study is to demonstrate favorable changes of periodontal endpoints in response to mechanical periodontal therapy in patients with generalized chronic periodontitis who completely switched to THS use compared with continued cigarette smoking.

Methods: This is a randomized controlled two-arm parallel-group multicenter Japanese study conducted in patients with chronic generalized periodontitis who switch from cigarettes to THS compared with smokers continuing to smoke cigarettes for 6 months. The patients were treated with mechanical periodontal therapy as per standard of care in Japan. The primary objective of the study is to demonstrate the beneficial effect of switching to THS use compared with continued cigarette smoking on pocket depth (PD) reduction in all sites with an initial PD≥4 mm. The secondary objectives include evaluation of other periodontal parameters (eg, clinical attachment level or gingival inflammation) and overall oral health status upon switching to THS. Safety was monitored throughout the study.

Results: In total, 172 subjects were randomized to the cigarette (n=86) or THS (n=86) groups, and all 172 completed the study. The conduct phase of the study is completed, while data cleaning and analyses are ongoing.

Conclusions: This study is the first to test a heat-not-burn tobacco product in smokers with an already established disease. The results should further strengthen the evidence that switching to THS can significantly reduce the risk of smoking-related diseases if favorable changes in the evolution of chronic generalized periodontitis after mechanical therapy are found when compared with continued cigarette smoking.

Trial registration: ClinicalTrials.gov NCT03364751; https://ichgcp.net/clinical-trials-registry/NCT03364751.

International registered report identifier (irrid): DERR1-10.2196/15350.

Keywords: Tobacco Heating System; clinical attachment level; modified risk tobacco product; oral health; periodontal pocket; periodontitis; probing depth; smoking; tobacco.

Conflict of interest statement

Conflicts of Interest: The work reported in this publication involved a candidate reduced risk product developed by PMI Research & Development. All authors are employees of PMI. PMI is the sole source of funding and sponsor of this project.

©Sandrine Pouly, Wee Teck Ng, Muriel Benzimra, Alexandre Soulan, Nicolas Blanc, Filippo Zanetti, Patrick Picavet, Gizelle Baker, Christelle Haziza. Originally published in JMIR Research Protocols (http://www.researchprotocols.org), 18.01.2021.

Figures

Figure 1
Figure 1
Design of the study. Eligibility criteria were checked at V1. Enrolled subjects were randomized at V2. Periodontal assessments were performed at V1, V3, and V4. Times of collection of buccal samples are indicated on the chart. BS: buccal swabs; GCF: gingival crevicular fluid; mo: month; SP: subgingival plaque; SRP: scaling and root planing; V: visit; THS: Tobacco Heating System.
Figure 2
Figure 2
Product use classification tree. Cig: cigarette; HS: HeatSticks.

References

    1. Johannsen A, Susin C, Gustafsson A. Smoking and inflammation: evidence for a synergistic role in chronic disease. Periodontol 2000. 2014 Feb;64(1):111–126. doi: 10.1111/j.1600-0757.2012.00456.x.
    1. Ojima M, Hanioka T, Tanaka K, Inoshita E, Aoyama H. Relationship between smoking status and periodontal conditions: findings from national databases in Japan. J Periodontal Res. 2006 Dec;41(6):573–579. doi: 10.1111/j.1600-0765.2006.00915.x.
    1. Torrungruang K, Nisapakultorn K, Sutdhibhisal S, Tamsailom S, Rojanasomsith K, Vanichjakvong O, Prapakamol S, Premsirinirund T, Pusiri T, Jaratkulangkoon O, Kusump S, Rajatanavin R. The effect of cigarette smoking on the severity of periodontal disease among older Thai adults. J Periodontol. 2005 Apr;76(4):566–572. doi: 10.1902/jop.2005.76.4.566.
    1. Warnakulasuriya S, Dietrich T, Bornstein MM, Casals Peidró E, Preshaw PM, Walter C, Wennström JL, Bergström J. Oral health risks of tobacco use and effects of cessation. Int Dent J. 2010 Feb;60(1):7–30. doi: 10.1922/IDJ_2532Warnakulasuriya24.
    1. Kaldahl WB, Johnson GK, Patil KD, Kalkwarf KL. Levels of cigarette consumption and response to periodontal therapy. J Periodontol. 1996 Jul;67(7):675–681. doi: 10.1902/jop.1996.67.7.675.
    1. US Department of Health and Human Services . The Health Consequences of Smoking—50 Years of Progress: A Report of the Surgeon General. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health; 2014. [2020-12-28]. .
    1. Yanagisawa T, Ueno M, Shinada K, Ohara S, Wright FAC, Kawaguchi Y. Relationship of smoking and smoking cessation with oral health status in Japanese men. J Periodontal Res. 2010 Apr;45(2):277–283. doi: 10.1111/j.1600-0765.2009.01233.x.
    1. Rodgman A, Perfetti TA. The chemical components of tobacco and tobacco smoke, 2nd Edition. Boca Raton, FL: CRC Press; 2013.
    1. Schaller JP, Keller D, Poget L, Pratte P, Kaelin E, McHugh D, Cudazzo G, Smart D, Tricker AR, Gautier L, Yerly M, Reis Pires R, Le Bouhellec S, Ghosh D, Hofer I, Garcia E, Vanscheeuwijck P, Maeder S. Evaluation of the Tobacco Heating System 2.2. Part 2: Chemical composition, genotoxicity, cytotoxicity, and physical properties of the aerosol. Regul Toxicol Pharmacol. 2016 Nov 30;81(Suppl 2):S27–S47. doi: 10.1016/j.yrtph.2016.10.001.
    1. Tymkiw KD, Thunell DH, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, Brogden KA, Guthmiller JM. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J Clin Periodontol. 2011 Mar;38(3):219–228. doi: 10.1111/j.1600-051X.2010.01684.x.
    1. Zambon J, Grossi S, Machtei E, Ho A, Dunford R, Genco R. Cigarette smoking increases the risk for subgingival infection with periodontal pathogens. J Periodontol. 1996 Oct;67(10 Suppl):1050–1054. doi: 10.1902/jop.1996.67.10s.1050.
    1. Teles R, Teles F, Frias-Lopez J, Paster B, Haffajee A. Lessons learned and unlearned in periodontal microbiology. Periodontol 2000. 2013 Jun;62(1):95–162. doi: 10.1111/prd.12010.
    1. Labriola A, Needleman I, Moles DR. Systematic review of the effect of smoking on nonsurgical periodontal therapy. Periodontol 2000. 2005;37:124–137. doi: 10.1111/j.1600-0757.2004.03793.x.
    1. Rivera-Hidalgo F. Smoking and periodontal disease. Periodontol 2000. 2003;32:50–58. doi: 10.1046/j.0906-6713.2003.03205.x.
    1. Grossi SG, Zambon J, Machtei EE, Schifferle R, Andreana S, Genco RJ, Cummins D, Harrap G. Effects of smoking and smoking cessation on healing after mechanical periodontal therapy. J Am Dent Assoc. 1997 May;128(5):599–607. doi: 10.14219/jada.archive.1997.0259.
    1. Nair P, Sutherland G, Palmer RM, Wilson RF, Scott DA. Gingival bleeding on probing increases after quitting smoking. J Clin Periodontol. 2003 May;30(5):435–437. doi: 10.1034/j.1600-051x.2003.20039.x.
    1. Morozumi T, Kubota T, Sato T, Okuda K, Yoshie H. Smoking cessation increases gingival blood flow and gingival crevicular fluid. J Clin Periodontol. 2004 Apr;31(4):267–272. doi: 10.1111/j.1600-051X.2004.00476.x.
    1. Luzzi LIT, Greghi SLA, Passanezi E, Sant'ana ACP, Lauris JRP, Cestari TM. Evaluation of clinical periodontal conditions in smokers and non-smokers. J Appl Oral Sci. 2007 Dec;15(6):512–517. doi: 10.1590/s1678-77572007000600011.
    1. Chambrone L, Preshaw PM, Rosa EF, Heasman PA, Romito GA, Pannuti CM, Tu Y. Effects of smoking cessation on the outcomes of non-surgical periodontal therapy: a systematic review and individual patient data meta-analysis. J Clin Periodontol. 2013 Jun;40(6):607–615. doi: 10.1111/jcpe.12106.
    1. Leite FRM, Nascimento GG, Baake S, Pedersen LD, Scheutz F, López R. Impact of Smoking Cessation on Periodontitis: A Systematic Review and Meta-analysis of Prospective Longitudinal Observational and Interventional Studies. Nicotine Tob Res. 2019 Nov 19;21(12):1600–1608. doi: 10.1093/ntr/nty147.
    1. Alexandridi F, Tsantila S, Pepelassi E. Smoking cessation and response to periodontal treatment. Aust Dent J. 2018 Jun;63(2):140–149. doi: 10.1111/adj.12568.
    1. Al Harthi SS, Natto ZS, Midle JB, Gyurko R, O'Neill R, Steffensen B. Association between time since quitting smoking and periodontitis in former smokers in the National Health and Nutrition Examination Surveys (NHANES) 2009 to 2012. J Periodontol. 2019 Jan;90(1):16–25. doi: 10.1002/JPER.18-0183.
    1. Preshaw PM, Heasman L, Stacey F, Steen N, McCracken GI, Heasman PA. The effect of quitting smoking on chronic periodontitis. J Clin Periodontol. 2005 Aug;32(8):869–879. doi: 10.1111/j.1600-051X.2005.00779.x.
    1. Rosa EF, Corraini P, de Carvalho VF, Inoue G, Gomes EF, Lotufo JPB, De Micheli G, Pannuti CM. A prospective 12-month study of the effect of smoking cessation on periodontal clinical parameters. J Clin Periodontol. 2011 Jun;38(6):562–571. doi: 10.1111/j.1600-051X.2011.01723.x.
    1. Holliday R, Preshaw PM, Ryan V, Sniehotta FF, McDonald S, Bauld L, McColl E. A feasibility study with embedded pilot randomised controlled trial and process evaluation of electronic cigarettes for smoking cessation in patients with periodontitis. Pilot Feasibility Stud. 2019;5:74. doi: 10.1186/s40814-019-0451-4.
    1. Ramôa CP, Eissenberg T, Sahingur SE. Increasing popularity of waterpipe tobacco smoking and electronic cigarette use: Implications for oral healthcare. J Periodontal Res. 2017 Oct;52(5):813–823. doi: 10.1111/jre.12458.
    1. Holliday RS, Campbell J, Preshaw PM. Effect of nicotine on human gingival, periodontal ligament and oral epithelial cells. A systematic review of the literature. J Dent. 2019 Jul;86:81–88. doi: 10.1016/j.jdent.2019.05.030.
    1. Malhotra R, Kapoor A, Grover V, Kaushal S. Nicotine and periodontal tissues. J Indian Soc Periodontol. 2010 Jan;14(1):72–79. doi: 10.4103/0972-124X.65442.
    1. Sundar IK, Javed F, Romanos GE, Rahman I. E-cigarettes and flavorings induce inflammatory and pro-senescence responses in oral epithelial cells and periodontal fibroblasts. Oncotarget. 2016 Nov 22;7(47):77196–77204. doi: 10.18632/oncotarget.12857.
    1. Javed F, Kellesarian SV, Sundar IK, Romanos GE, Rahman I. Recent updates on electronic cigarette aerosol and inhaled nicotine effects on periodontal and pulmonary tissues. Oral Dis. 2017 Nov;23(8):1052–1057. doi: 10.1111/odi.12652.
    1. Wadia R, Booth V, Yap HF, Moyes DL. A pilot study of the gingival response when smokers switch from smoking to vaping. Br Dent J. 2016 Dec 09;221(11):722–726. doi: 10.1038/sj.bdj.2016.914.
    1. Plessas A. Nonsurgical periodontal treatment: review of the evidence. Oral Health Dent Manag. 2014 Mar;13(1):71–80.
    1. Petersen PE. Tobacco and oral health--the role of the world health organization. Oral Health Prev Dent. 2003;1(4):309–315.
    1. World Health Organization . WHO Monograph on Tobacco Cessation and Oral Health Integration. Geneva: World Health Organization; 2017.
    1. Japanese society of periodontology clinical practice guideline for the periodontal treatment. Japanese Society of Periodontology. [2017-07-14]. .
    1. Ramseier CA. Smoking prevention and cessation. Oral Health Prev Dent. 2003;1(Suppl 1):427–39; discussion 440.
    1. Ramseier CA, Christen A, McGowan J, McCartan B, Minenna L, Ohrn K, Walter C. Tobacco use prevention and cessation in dental and dental hygiene undergraduate education. Oral Health Prev Dent. 2006;4(1):49–60.
    1. Lüdicke F, Picavet P, Baker G, Haziza C, Poux V, Lama N, Weitkunat R. Effects of Switching to the Tobacco Heating System 2.2 Menthol, Smoking Abstinence, or Continued Cigarette Smoking on Biomarkers of Exposure: A Randomized, Controlled, Open-Label, Multicenter Study in Sequential Confinement and Ambulatory Settings (Part 1) Nicotine Tob Res. 2018 Jan 05;20(2):161–172. doi: 10.1093/ntr/ntw287.
    1. Haziza C, de La Bourdonnaye G, Donelli A, Poux V, Skiada D, Weitkunat R, Baker G, Picavet P, Lüdicke F. Reduction in Exposure to Selected Harmful and Potentially Harmful Constituents Approaching Those Observed Upon Smoking Abstinence in Smokers Switching to the Menthol Tobacco Heating System 2.2 for 3 Months (Part 1) Nicotine Tob Res. 2020 Apr 17;22(4):539–548. doi: 10.1093/ntr/ntz013.
    1. Haziza C, de La Bourdonnaye G, Merlet S, Benzimra M, Ancerewicz J, Donelli A, Baker G, Picavet P, Lüdicke F. Assessment of the reduction in levels of exposure to harmful and potentially harmful constituents in Japanese subjects using a novel tobacco heating system compared with conventional cigarettes and smoking abstinence: A randomized controlled study in confinement. Regul Toxicol Pharmacol. 2016 Nov;81:489–499. doi: 10.1016/j.yrtph.2016.09.014.
    1. Haziza C, de La Bourdonnaye G, Skiada D, Ancerewicz J, Baker G, Picavet P, Lüdicke F. Evaluation of the Tobacco Heating System 2.2. Part 8: 5-Day randomized reduced exposure clinical study in Poland. Regul Toxicol Pharmacol. 2016 Nov;81(Suppl.2):S139–S150. doi: 10.1016/j.yrtph.2016.11.003.
    1. US Institute of Medicine . Scientific standards for studies on modified risk tobacco products. Washington, DC: The National Academies Press; 2012.
    1. US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health . How tobacco smoke causes disease: The biology and behavioral basis for smoking-attributable disease: A report of the surgeon general. Atlanta, GA: Centers for Disease Control and Prevention; 2010.
    1. Lüdicke F, Picavet P, Baker G, Haziza C, Poux V, Lama N, Weitkunat R. Effects of Switching to the Menthol Tobacco Heating System 2.2, Smoking Abstinence, or Continued Cigarette Smoking on Clinically Relevant Risk Markers: A Randomized, Controlled, Open-Label, Multicenter Study in Sequential Confinement and Ambulatory Settings (Part 2) Nicotine Tob Res. 2018 Jan 05;20(2):173–182. doi: 10.1093/ntr/ntx028.
    1. Ansari SM, Lama N, Blanc N, Bosilkovska M, Donelli A, Picavet P, Baker G, Haziza C, Lüdicke F. Evaluation of Biological and Functional Changes in Healthy Smokers Switching to the Tobacco Heating System 2.2 Versus Continued Tobacco Smoking: Protocol for a Randomized, Controlled, Multicenter Study. JMIR Res Protoc. 2018 Aug 24;7(8):e11294. doi: 10.2196/11294.
    1. Zanetti F, Titz B, Sewer A, Lo Sasso G, Scotti E, Schlage WK, Mathis C, Leroy P, Majeed S, Torres LO, Keppler BR, Elamin A, Trivedi K, Guedj E, Martin F, Frentzel S, Ivanov NV, Peitsch MC, Hoeng J. Comparative systems toxicology analysis of cigarette smoke and aerosol from a candidate modified risk tobacco product in organotypic human gingival epithelial cultures: A 3-day repeated exposure study. Food Chem Toxicol. 2017 Mar;101:15–35. doi: 10.1016/j.fct.2016.12.027.
    1. Iskandar AR, Titz B, Sewer A, Leroy P, Schneider T, Zanetti F, Mathis C, Elamin A, Frentzel S, Schlage WK, Martin F, Ivanov NV, Peitsch MC, Hoeng J. Systems toxicology meta-analysis of assessment studies: biological impact of a candidate modified-risk tobacco product aerosol compared with cigarette smoke on human organotypic cultures of the aerodigestive tract. Toxicol Res (Camb) 2017 Sep 01;6(5):631–653. doi: 10.1039/c7tx00047b.
    1. Guideline for good clinical practice. ICH E6 (R1) [2014-08-14]. .
    1. Integrated addendum to ICH E6 (R1): Guideline for good clinical practice - current step 4 version dated 9 november 2016. International Council for Harmonisation of Technical Requirements for Pharmaceuticals for Human Use (ICH) E6 (R2) 2016. Nov 09, [2016-01-17]. .
    1. Ministerial ordinance on good clinical practice for drugs. Ordinance of the Ministry of Health and Welfare No. 28. 1997. Mar 27, [2013-01-17]. .
    1. Declaration of Helsinki - ethical principles for medical research involving human subjects. World Medical Association (WMA) [2018-07-12].
    1. Calsina G, Ramón JM, Echeverría JJ. Effects of smoking on periodontal tissues. J Clin Periodontol. 2002 Aug;29(8):771–776. doi: 10.1034/j.1600-051x.2002.290815.x.
    1. Machtei EE, Hausmann E, Schmidt M, Grossi SG, Dunford R, Schifferle R, Munoz K, Davies G, Chandler J, Genco RJ. Radiographic and clinical responses to periodontal therapy. J Periodontol. 1998 May;69(5):590–595. doi: 10.1902/jop.1998.69.5.590.
    1. Haffajee AD, Socransky SS, Dibart S, Kent RL. Response to periodontal therapy in patients with high or low levels of P. gingivalis, P. intermedia, P. nigrescens and B. forsythus. J Clin Periodontol. 1996 Apr;23(4):336–345. doi: 10.1111/j.1600-051x.1996.tb00555.x.
    1. Preber H, Bergström J. Cigarette smoking in patients referred for periodontal treatment. Scand J Dent Res. 1986 Apr;94(2):102–108. doi: 10.1111/j.1600-0722.1986.tb01372.x.
    1. Liu KH, Hwang SJ. Effect of smoking cessation for 1 year on periodontal biomarkers in gingival crevicular fluid. J Periodontal Res. 2016 Jun;51(3):366–375. doi: 10.1111/jre.12316.
    1. Hackshaw A, Morris JK, Boniface S, Tang J, Milenković D. Low cigarette consumption and risk of coronary heart disease and stroke: meta-analysis of 141 cohort studies in 55 study reports. BMJ. 2018 Jan 24;360:j5855. doi: 10.1136/bmj.j5855.
    1. Bjartveit K, Tverdal A. Health consequences of smoking 1-4 cigarettes per day. Tob Control. 2005 Oct;14(5):315–320. doi: 10.1136/tc.2005.011932.
    1. Smiley CJ, Tracy SL, Abt E, Michalowicz BS, John MT, Gunsolley J, Cobb CM, Rossmann J, Harrel SK, Forrest JL, Hujoel PP, Noraian KW, Greenwell H, Frantsve-Hawley J, Estrich C, Hanson N. Evidence-based clinical practice guideline on the nonsurgical treatment of chronic periodontitis by means of scaling and root planing with or without adjuncts. J Am Dent Assoc. 2015 Jul;146(7):525–535. doi: 10.1016/j.adaj.2015.01.026.
    1. Miller PD. A classification of marginal tissue recession. Int J Periodontics Restorative Dent. 1985;5(2):8–13.
    1. Löe H. The Gingival Index, the Plaque Index and the Retention Index Systems. J Periodontol. 1967;38(Suppl 6):610–616. doi: 10.1902/jop.1967.38.6.610.
    1. Preshaw PM, Lauffart B, Zak E, Jeffcoat MK, Barton I, Heasman PA. Progression and treatment of chronic adult periodontitis. J Periodontol. 1999 Oct;70(10):1209–1220. doi: 10.1902/jop.1999.70.10.1209.
    1. Rosa EF, Corraini P, Inoue G, Gomes EF, Guglielmetti MR, Sanda SR, Lotufo JPB, Romito GA, Pannuti CM. Effect of smoking cessation on non-surgical periodontal therapy: results after 24 months. J Clin Periodontol. 2014 Dec;41(12):1145–1153. doi: 10.1111/jcpe.12313.
    1. Fiorini T. Smoking cessation may promote additional benefits to non-surgical periodontal therapy in adults with chronic periodontitis. J Evid Based Dent Pract. 2015 Jun;15(2):83–84. doi: 10.1016/j.jebdp.2015.03.015.
    1. Fiorini T, Musskopf ML, Oppermann RV, Susin C. Is there a positive effect of smoking cessation on periodontal health? A systematic review. J Periodontol. 2014 Jan;85(1):83–91. doi: 10.1902/jop.2013.130047.
    1. Hughes FJ, Syed M, Koshy B, Bostanci N, McKay IJ, Curtis MA, Marcenes W, Croucher RE. Prognostic factors in the treatment of generalized aggressive periodontitis: II. Effects of smoking on initial outcome. J Clin Periodontol. 2006 Sep;33(9):671–676. doi: 10.1111/j.1600-051X.2006.00965.x.
    1. Nasry HA, Preshaw PM, Stacey F, Heasman L, Swan M, Heasman PA. Smoking cessation advice for patients with chronic periodontitis. Br Dent J. 2006 Mar 11;200(5):272–275; discussion 265. doi: 10.1038/sj.bdj.4813307.
    1. Ramseier CA, Bornstein MM, Saxer UP, Klingler K, Walter C. Tobacco use prevention and cessation in the dental practice. Schweiz Monatsschr Zahnmed. 2007;117(3):253–278.
    1. Christen AG. Tobacco cessation, the dental profession, and the role of dental education. J Dent Educ. 2001 Apr;65(4):368–374.
    1. Hilgers KK, Kinane DF. Smoking, periodontal disease and the role of the dental profession. Int J Dent Hyg. 2004 May;2(2):56–63. doi: 10.1111/j.1601-5029.2004.00075.x.
    1. Leroy R, Eaton KA, Savage A. Methodological issues in epidemiological studies of periodontitis--how can it be improved? BMC Oral Health. 2010 Apr 21;10:8. doi: 10.1186/1472-6831-10-8.
    1. Andrade R, Espinoza M, Gómez EM, Espinoza JR, Cruz E. Intra- and inter-examiner reproducibility of manual probing depth. Braz Oral Res. 2012;26(1):57–63. doi: 10.1590/s1806-83242012000100010.
    1. Hefti AF, Preshaw PM. Examiner alignment and assessment in clinical periodontal research. Periodontol 2000. 2012 Jun;59(1):41–60. doi: 10.1111/j.1600-0757.2011.00436.x.
    1. Dietrich T, Bernimoulin J, Glynn RJ. The effect of cigarette smoking on gingival bleeding. J Periodontol. 2004 Jan;75(1):16–22. doi: 10.1902/jop.2004.75.1.16.
    1. Javed F, Abduljabbar T, Vohra F, Malmstrom H, Rahman I, Romanos GE. Comparison of Periodontal Parameters and Self-Perceived Oral Symptoms Among Cigarette Smokers, Individuals Vaping Electronic Cigarettes, and Never-Smokers. J Periodontol. 2017 Oct;88(10):1059–1065. doi: 10.1902/jop.2017.170197.
    1. Huilgol P, Bhatt SP, Biligowda N, Wright NC, Wells JM. Association of e-cigarette use with oral health: a population-based cross-sectional questionnaire study. J Public Health (Oxf) 2019 Jun 01;41(2):354–361. doi: 10.1093/pubmed/fdy082.
    1. BinShabaib M, Al Harthi SS, Akram Z, Khan J, Rahman I, Romanos GE, Javed F. Clinical periodontal status and gingival crevicular fluid cytokine profile among cigarette-smokers, electronic-cigarette users and never-smokers. Arch Oral Biol. 2019 Jun;102:212–217. doi: 10.1016/j.archoralbio.2019.05.001.
    1. Al Harthi SS, BinShabaib M, Akram Z, Rahman I, Romanos GE, 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 Jun;23(6):2751–2758. doi: 10.1007/s00784-018-2725-2.

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