Periodontal and Peri-Implant Health Status in Traditional vs. Heat-Not-Burn Tobacco and Electronic Cigarettes Smokers: A Systematic Review
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dentistry journal
Systematic Review
Periodontal and Peri-Implant Health Status in Traditional vs.
Heat-Not-Burn Tobacco and Electronic Cigarettes Smokers:
A Systematic Review
Francesco D’Ambrosio * , Massimo Pisano, Alessandra Amato, Alfredo Iandolo, Mario Caggiano
and Stefano Martina
Department of Medicine, Surgery and Dentistry “Schola Medica Salernitana”, University of Salerno,
Via S. Allende, 84081 Baronissi, Italy; pisano.studio@virgilio.it (M.P.); aamato@unisa.it (A.A.);
aiandolo@unisa.it (A.I.); macaggiano@unisa.it (M.C.); smartina@unisa.it (S.M.)
* Correspondence: francesco87fd@libero.it
Abstract: The aim of the present systematic review was to evaluate and possibly differentiate the
effects of traditional cigarettes, heat-not-burn tobacco, and electronic cigarettes on periodontal and
peri-implant health status. Electronic cigarettes and heat-not-burn tobacco have become very popular
in recent years and have been proposed to consumers as a safer alternative to conventional tobacco
smoke, although their effect on periodontal and peri-implant health remains unclear. The study
protocol was developed according to PRISMA guidelines, and the focus question was formulated
according to the PICO strategy. A literature search was conducted across PubMed/MEDLINE and the
COCHRANE library from 2003 to April 2022. From the 1935 titles initially identified, 18 articles were
finally included in the study and extracted data were qualitatively synthesized. It may be carefully
Citation: D’Ambrosio, F.; Pisano, M.;
concluded that e-cigarettes may cause attenuated clinical inflammatory signs of periodontitis and,
Amato, A.; Iandolo, A.; Caggiano, M.; hypothetically, of peri-implantitis when compared to conventional tobacco smoke. Both alternative
Martina, S. Periodontal and smoking products, containing nicotine, may likewise exert negative effects on periodontal and peri-
Peri-Implant Health Status in implant health, as demonstrated by in vitro studies. Further investigations are needed to assess the
Traditional vs. Heat-Not-Burn impact of electronic cigarettes and heat-not-burn tobacco products on periodontal and peri-implant
Tobacco and Electronic Cigarettes health status.
Smokers: A Systematic Review. Dent.
J. 2022, 10, 103. https://doi.org/ Keywords: tobacco; cigarette smoking; smokers; electronic cigarettes; electronic nicotine delivery
10.3390/dj10060103 system; E-Cigs; periodontal disease; periodontitis; peri-implant disease; peri-implantitis
Academic Editor: Jesus Torres
Garcia-Denche
Received: 18 May 2022
1. Introduction
Accepted: 31 May 2022
Published: 8 June 2022
Periodontitis is a chronic inflammatory disease of bacterial etiology, affecting and pro-
gressively destroying the tissues supporting the teeth and eventually leading to bone and
Publisher’s Note: MDPI stays neutral
tooth loss [1–5]. Analogously, peri-implantitis is an inflammatory lesion of the soft tissues
with regard to jurisdictional claims in
surrounding an endosseous implant, leading to progressive peri-implant bone loss until
published maps and institutional affil-
implant failure [1–5]. Both periodontal and peri-implant diseases most frequently occur in
iations.
adulthood and have been found or proposed to be associated, mainly through systemic
inflammation, to a variety of systemic inflammatory disorders, including cardiovascular
and pulmonary ones, diabetes, obesity, preterm birth, Alzheimer disease, and benign and
Copyright: © 2022 by the authors.
solid malignant tumors [6–11].
Licensee MDPI, Basel, Switzerland. Although periodontitis and peri-implantitis are both bacterial infections involving den-
This article is an open access article tal biofilm, suspected periodontal pathogens, individual age at disease onset, periodontitis
distributed under the terms and severity, and rate of progression are all crucially influenced by well-known systemic factors,
conditions of the Creative Commons including inflammatory disorders—most importantly diabetes [6–10]—and neoplasms [11],
Attribution (CC BY) license (https:// as well as unhealthy habits [12], especially smoking [13,14].
creativecommons.org/licenses/by/ Electronic cigarettes (E-Cigs) were introduced in the United States of America in 2006
4.0/). and, since 2014, have become the most widespread tobacco product among young people
Dent. J. 2022, 10, 103. https://doi.org/10.3390/dj10060103 https://www.mdpi.com/journal/dentistryDent. J. 2022, 10, 103 2 of 35
between 18 and 25 years of age as a pastime [15], as well as among adults as an alternative
to regular tobacco cigarettes and to quit smoking [16], similarly to the heat-not-burn (HNB)
tobacco products that are becoming a new global trend [17].
E-cigarettes are small handheld devices containing a battery heating a solution and
producing an aerosol. Usually, the liquid contains a mixture of substances such as nicotine,
humectants, and flavoring chemical agents [18,19]. However, traces of heavy metals, such
as aluminum, arsenic, nickel, and other contaminants very dangerous for human health
have been found [20].Accordingly, Gaur and Agnihotri demonstrated that E-Cig use, also
referred to as “vaping”, is not a safe alternative to normal tobacco cigarettes because the
vaping liquid itself contains elements and toxic heavy metals predisposing the user to
chronic pathological conditions [21].
Moreover, Rahlo et al. and Yang et al. concluded that although electronic cigarette
users may somehow be considered healthier than conventional cigarette smokers, they are
still predisposed to the development of oral mucosal lesions and to dental and periodontal
damage compared to non-smokers [22]. Figueredo et al., based on limited data available,
reported that e-cigarettes have an unhealthy effect on periodontal health [23]. Similarly,
Jeong et al., evaluating periodontal health status in 13,551 conventional and E-Cig smokers,
concluded that electronic cigarette vaping and conventional cigarette smoking were both
risk factors for periodontal diseases [24].
Furthermore, results from in vitro studies showed that E-Cig use is capable of alter-
ing myofibroblasts differentiation, causing DNA damage, inducing oxidative stress, and
increasing inflammatory cytokines in human gingiva and periodontal ligament fibrob-
lasts [25]. A recent study has also shown that the concentrations of both albumin and uric
acid detectable in the whole saliva differ between smokers and non-smokers, being reduced
in non-smokers [26].
Tobacco heating systems instead employ a particular heating method, reaching lower
temperatures (240–350 ◦ C) compared to traditional tobacco (>600 ◦ C) [26], thus avoiding
combustion. To our knowledge, only one study, not considering self-reported periodon-
titis, has presented provisional results describing more favorable periodontal treatment
outcomes in HNB compared to conventional tobacco smokers [27]; however, it has been
reported that HNB tobacco may potentially enhance oral epithelial cell proliferation [28].
Considering that both E-Cigs and HNB tobacco are proposed to consumers as less
harmful compared to traditional cigarettes and as a safer alternative to conventional
tobacco [26], a comparison of their effect on periodontal and peri-implant health status,
while also evaluating former or current traditional tobacco smokers, may be especially
relevant, both in the prevention and treatment planning of periodontal and peri-implant
diseases. Therefore, the aim of the present systematic review was to evaluate and possibly
differentiate the effects of conventional cigarettes, electronic cigarettes, and heat-not-burn
tobacco products on periodontal and peri-implant status.
2. Materials and Methods
2.1. Protocol Development
The study protocol was developed according to the PRISMA (Preferred Reporting
Items for Systematic Review and Meta-Analyses) guidelines [29,30]. The research question
was formulated according to the PICO (Population, Intervention, control or Comparison,
Outcome) strategy [31]:
P (Population): Smokers;
I (Intervention): Electronic cigarettes and heat-not-burn tobacco systems;
C (Comparison): Non-smokers, ex-smokers, and tobacco cigarette smokers;
O (Outcome): Clinical, radiographic, and inflammatory periodontal and peri-implant
tissue parameters.
The clinical question in “PICO” format was: Is there a significant difference in clinical,
radiographic and inflammatory parameters of periodontal and peri-implant tissues fromDent. J. 2022, 10, 103 3 of 35
e-cigarette users and Heat-Not-Burn tobacco when compared to tobacco users and non-
smoking subjects?
2.2. Search Strategy and Study Selection
A literature search was independently conducted by two reviewers (F.D.A., S.M.)
through PubMed/MEDLINE and the COCHRANE library. Only articles published after
1st January 2003 (when the electronic cigarette was introduced) till 24th April 2022, in the
English language, were included.
A combination of the following keywords was employed for the electronic search:
Periodontal disease OR periodontitis OR peri-implant disease OR peri-implantitis
OR dental implant OR implant loss OR plaque index OR gingival index OR bleeding on
probing OR probing depth OR tooth loss OR missing teeth OR marginal bone level OR
IL-1b OR IL-8 OR IL-6 OR TNF-a OR MMP-1 OR MMP-8 OR IFN-y OR IL-4 OR IL-9
OR IL-10 OR IL-13 OR OPG OR RANK-LAND OR e-cigarette OR vaping cigarette OR
electronic cigarette OR electronic nicotine delivery system OR Heat-Not-Burn Tobacco OR
vape OR vaping.
Articles were included if they were published in the English language, after 1st January
2003, and described clinical trials and/or observational studies assessing clinical and/or
radiographic periodontal and/or peri-implant parameters. Records were excluded if study
participants wereDent. J. 2022, 10, 103 4 of 35
because duplicates and 1796 titles were excluded as they were not pertinent to the topic
of the present review; therefore, 41 articles were considered eligible and full texts were
obtained. After the full-text evaluation according to the selection criteria, 23 studies
were excluded (Table 1), specifically because: 11 did not describe clinical/radiographic
parameters nor cytokine profile (11); 2 exclusively investigated the relationship between
e-cigarettes and oral microbiome and 1 between e-cigarettes and alcohol, respectively;
2 studies involved former tobacco smokers who started using E-Cigs; 1 study assessed
the effect of antimicrobial photodynamic therapy (aPDT) in E-Cigs smokers; and 6 articles
were systematic reviews of the literature.
Table 1. Excluded studies and reason for exclusion.
Authors, Year Reason for Exclusion
Yang, 2020 [23] Systematic review
Ralho, 2019 [22] Systematic review
Javed, 2017 [33] No clinical/radiographic parameters
Shaito, 2017 [34] No clinical/radiographic parameters
Vyncke, 2020 [35] Systematic review
Karina, 2020 [36] Review
Atuegwu, 2019 [37] No clinical/radiographic parameters
Chrcanovic, 2015 [11] Systematic review
Sancilio, 2015 [38] No clinical/radiographic parameters
Ryder, 2018 [12] Relationship between e-cigarettes and alcohol
Javed, 2019 [39] No clinical/radiographic parameters
Ganesan, 2020 [40] Relationship between e-cigarettes and oral microbiome
Andrikopoulos, 2019 [41] No clinical/radiographic parameters
Nelson, 2019 [42] Relationship between e-cigarettes and oral microbiome
Willershausen, 2014 [43] No clinical/radiographic parameters
Rouabhia, 2018 [44] No clinical/radiographic parameters
Holliday, 2019 [45] Study on tobacco cessation and starting e-cigarettes
Zanetti, 2016 [46] No clinical/radiographic parameters
Sandar, 2016 [27] No clinical/radiographic parameters
Study on tobacco smokers which started to use
Tatullo, 2016 [47]
E-cigarette
Alqahtani, 2020 [48] No clinical/radiographic parameters
Effect of the antimicrobial photodynamic therapy
Al Rifaiy, 2018 [49]
(aPDT) individuals vaping electronic cigarettes
Figueredo, 2021 [25] Systematic review
Finally, 18 articles were included in the present systematic review (Figure 1).Dent.J. J.2022,
Dent. 2022,10,
10,103
x FOR PEER REVIEW 55 of
of3525
Figure 1. Study selection flowchart.
Figure 1. Study selection flowchart.
3.2.Study
3.2. StudyCharacteristics
Characteristics
Table2 2illustrates
Table illustratesthethecharacteristics
characteristicsofofthethe1818included
includedstudies,
studies,concerning
concerningsource,
source,
study
studydesign,
design,aim(s),
aim(s),participants,
participants,periodontal
periodontaland andperi-implant
peri-implantparameters
parametersconsidered,
considered,
main
mainresults
resultsandandconclusions.
conclusions.
All
Allincluded
included studies evaluated
studies periodontal
evaluated periodontalparameters
parametersand and
in 7 out
in 7ofout
18 peri-implants
of 18 peri-im-
were also
plants wereassessed. Extracted
also assessed. and analyzed
Extracted periodontal
and analyzed and peri-implant
periodontal and peri-implant parameters
parame-
concerned traditional and electronic cigarettes smokers, whilst no study
ters concerned traditional and electronic cigarettes smokers, whilst no study analyzed analyzed findings
from HNBfrom
findings tobacco
HNBsmokers; results from
tobacco smokers; waterpipe
results smokerssmokers
from waterpipe were also reported
were in the
also reported
synthesis of the results
in the synthesis of the and briefly
results and discussed, although
briefly discussed, not relevant
although for the present
not relevant study,
for the present
since they
study, could
since theynot be extrapolated
could from data
not be extrapolated comparison
from among study
data comparison among groups.
study groups.
Due
Dueto to the
the heterogeneity
heterogeneity of of the
theincluded
includedstudies
studiesandandto to
thethelacklack of randomized
of randomized con-
controlled trials, it was not possible to conduct a meta-analysis.
trolled trials, it was not possible to conduct a meta-analysis.Dent. J. 2022, 10, 103 6 of 35
Table 2. Characteristics of the studies included in the present systematic review: author(s) and year of publication; study design; total number, mean age, gender
ratio and smoking habits of participants; periodontal status, number of implants, and periodontal and peri-implant clinical, radiographic and crevicular parameters,
including clinical attachment loss (CAL) probing depth (PD), bleeding on probing (BoP), plaque index (PI), gingival index (GI), marginal bone levels (MBL),
cytokines profile and periodontal treatment. Electronic devices intended for “vaping” were heterogeneously defined by the authors of the included studies and are
currently named as “electronic cigarettes”.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
PI was significantly higher among CS
and WS than E-Cigs (p < 0.05) and NS
(p < 0.05).PI was significantly higher
among E-Cigs than NS (p < 0.05).
Periodontal and peri-implant BOP were significantly higher among
assessment at baseline NS compared with CS (p < 0.05) and
No periodontal treatment WS (p < 0.05) and E-Cigs (p < 0.05) CS and WS had worse radiographic
Mokeem, 2018
No dental implants PD (p < 0.05), CAL (p < 0.05) and MBL parameters of periodontal
[50] 39 CS (42.4 ± 5.6 y.o.)
PI (p < 0.05) were significantly higher inflammation than E-Cigs and NS.
Case-control 40 E-Cigs (44.7 ± 4.5 y.o.)
BoP among CS and WS compared with Cotinine levels were similar
To compare PI, BOP, PD, CAL, 37 E-Cigs (28.3 ± 3.5 y.o.)
CAL E-Cigs and NS. in all groups.
MBL and cotinine, interleukin 38NS (40.6 ± 4.5 y.o.)
PD There was no difference in PD, CAL, Salivary IL-1β and IL-6 levels were
IL-1β and IL-6 levels among CS, All males
MBL MBL, IL-1β and IL-6 levels among higher in CS and WS than E-Cigs
WS, E-Cigs and NS
IL-1b E-Cigs and NS and NS
IL-6 IL-1β (p < 0.01) and IL-6 (p < 0.01)
cotinine levels were significantly higher among
CS, WS than E-Cigs and NS.
Cotinine levels were significantly higher
among CS (p < 0.001) and WS (p < 0.001)
and E-Cigs (p < 0.001) than NS.Dent. J. 2022, 10, 103 7 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
Periodontal and peri-implant BOP was statistically significantly
assessment at baseline higher in NS compared to E-Cigs
No periodontal treatment (p < 0.01).
Al-Aali, 2018
Dental implants n. 125 (at least one PD (p < 0.05); PIBL (p < 0.05);TNF-a Clinical and radiographic
[51]
positioned for ≥36 months) (p < 0.001) and IL-1b (p < 0.01) were peri-implant parameters are worse
Case-control 47 E-Cigs (35.8 ± 6.2 y.o.)
PI statistically significantly higher in among E-Cigs than NS.
To compare clinical and 45 NS (42.6 ± 2.7 y.o.)
BoP E-Cigs than NS. E-Cigs show higher levels of
radiographic peri-implant All males
PD (>/=4 mm) There was a significant positive pro-inflammatory cytokines than
parameters and TNF-a and IL-1b
PIBL relationship among TNF-a levels and NS.
levels among E-Cigs and NS
TNF-α BOP (P5.024) and PIBL (P5.016); and
IL-1β among IL-1b and PIBL (P5.018) in
PISF volume E-Cigs.
Periodontal and peri-implant
No significant differences were found
Karaaslan, 2020 assessment at baseline
between the groups for PD, PI, CAL.
[52] No periodontal treatment
GI was significantly higher in group 2e
Case-control No dental implants
19 CS (35.26 ± 2.31 y.o.) 3 than group 1 and GI was significantly
To evaluate the effects of vaping, PI Cigarette smoke and vaping have
19 E-Cigs (34.74 ± 2.38 y.o.) lower in group 2 than group 3.
cigarettes smoke and smoking GI negative effects on the markers of
Ex- cigarettes smokers: 19 IL-8 level of Group I (70.47 ± 2.76) was
cessation on periodontal clinical CAL oxidative stress and inflammatory
individuals (35.58 ± 2.04 y.o.) significantly lower than in Groups II
parameters, oxidative stress IL-8 cytokines.
39M/18F and III.
markers and pro-inflammatory TNF-a
TNF-a level of Group I (4.20 ± 0.14) was
cytokines in patients with GsH-Px (Glutathione peroxidase)
significantly higher than in Groups II
periodontal disease 8-OHdG
and III.
(8-hydroxydeoxyguanosine)Dent. J. 2022, 10, 103 8 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
Periodontal and peri-implant Peri-implant PI (p < 0.05), PD (p < 0.05) and
assessment at baseline RBL (p < 0.01) was significantly higher
No periodontal treatment among CS, WS and E-Cigs compared to NS.
AlQahtani, 2018 Dental implants n. 253 (at least one BOP in CS, WS, and E-Cigs showed
40 CS
[53] in service for >/=36 months) statistical differences (p < 0.01) compared to
40 WS
Case-control PI NS
40 E-Cigs Tobacco smoking is associated with
To compare clinical and BoP CS and WS showed significantly higher PD
40 NS poor peri-implant health.
radiographic peri-implant PD (≥4 mm) ≥ 4 mm and RBL compared with E-Cigs
Mean age: 41.8 y.o.
parameters and cytokines among MBL (p < 0.05).
All males
CS, WS, E-Cigs, and NS TNF-a TNF-α, IL-6, and IL-1β were significantly
IL-6 higher in CS, WS, and E-Cigs than NS.
IL-1B No statistical differences for cytokines were
PISF observed among CS and WS.
Periodontal and peri-implant
assessment at baseline
PI (p < 0.05), PD (p < 0.05) and clinical
No periodontal treatment
AL (p < 0.05) were significantly higher
No dental implants
among individuals in CS than NS.
BinShabaib, 2019 PI
46 CS (29.5 ± 5.8 y.o.) BOP was manifested more among NS
[54] BoP
43M:3F than in CS (p < 0.05) and E-Cigs Periodontal status is worse and GCF
Case-control PD
44 E-Cigs (27.8 ± 3.1 y.o.) (p < 0.05). levels of pro-inflammatory
To compare clinical periodontal CAL
42M:2F MBL was significantly higher in CS cytokines are higher in CS
status and gingival crevicular MT
45NS (30.2 ± 4.4 y.o.) (p < 0.01) and E-Cigs (p < 0.01) than NS compared with E-Cigs and NS.
fluid cytokine profile among CS, MBL
39M:6F The concentrations of IL-1β, IL-6, IFN-γ,
E-Cigs and NS IL-1b
TNF-α and MMP-8 were significantly
IL-6
higher in the GCF samples of CS
TNF-a
(p < 0.05) than E-Cigs and NS.
MMP-8
IFN-gDent. J. 2022, 10, 103 9 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
Periodontal and peri-implant
assessment at baseline
Vohra, 2020
No periodontal treatment
[55] PI (p < 0.05) and PD (p < 0.05) were PI and PD are increased in CS than
28 CS (33.3 ± 2.2 y.o.) No dental implants
Case-control increased in CS than E-Cigs and NS. other groups.
26 E-Cigs (31.8 ± 2.05 y.o.) PI
To compare self-rated oral There was no statistically significant Pain in teeth and gums are more
26 NS (33.5 ± 1.4 y.o.) BoP
symptoms and clinical and difference in BOP, CAL, MBL and MT often perceived by CS than other
All males CAL
radiographic periodontal status among the four groups. groups.
PD (>/=4 mm)
among CS, E-Cigs, and NS
MT
MBL
Periodontal and peri-implant
assessment at baseline
PI (p < 0.01), and PD ≥ 4 mm (p < 0.01)
Javed, 2017 No periodontal treatment
were significantly higher in CS and in
[56] 33 CS (41.3 ± 2.8 y.o.) No dental implants
E-Cigs compared to NS. CS show worse clinical periodontal
Cohort 31 E-Cigs (37.6 ± 2.1 y.o.) PI
BOP was significantly higher in NS than parameters
To compare clinical periodontal 30 NS (40.7 ± 1.6 y.o.) BoP
CS (p < 0.01) and E-Cigs (p < 0.01). compared with E-Cigs and NS.
parameters among CS, E-Cigs and All males CAL
There was no difference in MT, CAL
NS PD (>/=4 mm)
and MBL among the groups.
MT
MBLDent. J. 2022, 10, 103 10 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
Total number: 13,551
With and without periodontal
Jeong, 2020 Periodontal and peri-implant
disease Periodontal disease was more prevalent E-Cigs and CS were significantly
[26] assessment at baseline (data
CS in E-Cigs and CS than NS. associated with increased
Case-control between 2013 and 2015)
E-Cigs E-Cigs and CS had higher dental periodontal disease. So, vaping may
To evaluate the association of CS No periodontal treatment
Ex-CS disease (dental caries, toothache and not be a healthy alternative to
and E-Cigs with periodontal No dental implants
NS dental damages) than NS. cigarette smoke.
disease CPI
≥18 y.o.
5715M/7836F
The scores of PI (p < 0.001), GI
Periodontal and peri-implant (p < 0.001), CAL (p < 0.001), PD
Aldakheel, 2020
15 CS (40.5 ± 2.1 y.o.) assessment: MD (p < 0.001) and mesial (p < 0.001) and
[57]
5 E-Cigs (38.6 ± 3.3 y.o.) No periodontal treatment distal (p < 0.001) MBL were significantly
Case-control
15NS with periodontitis (39.4 ± No dental implants higher among CS, E-Cigs, and NS with E-Cigs and CS have the same
To compare pathogenic bacteria,
1.6 y.o.) PI periodontitis compared with NS number of pathogenic bacteria in
count from the subgingival
15 NS without periodontitis (39.5 GI without periodontitis. There was no the oral-biofilm.
biofilm of CS and E-Cigs with
± 0.8 y.o.) PD statistically significant difference in GI,
periodontitis with that of NS with
M/F: MD CAL PD, CAL, mesial and distal MBL and PI
and without periodontitis
MBL among CS, E-Cigs, and NS with
periodontitis.Dent. J. 2022, 10, 103 11 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
PI (p < 0.01) and PD (p < 0.01) were
significantly higher among CS, WS,
E-Cigs than NS.
The GCF volume was significantly
higher among CS (0.92 ± 0.05 µL)
Periodontal and peri-implant (p < 0.01) and WS (0.66 ± 0.08 µL)
assessment: MD (p < 0.001) and E-Cigs (0.62 ± 0.03 µL)
Ibraheem, 2020
No periodontal treatment (p < 0.01) than NS (0.21 ± 0.007 µL).
[58]
30 CS (46.5 ±5.3 y.o.) No dental implants The RANKL levels were significantly
Case-control
30 WS (45.5 ±4.4 y.o.) PI higher among CS (14.9 ± 8.2 pg/mL) CS, WS and E-Cigs have higher
To compare the levels of Receptor
30 E-Cigs (45.6 ± 3.6 y.o.) BoP (p < 0.001) and WS (12.6 ± 8.8 pg/mL) levels of RANKL and OPG in the
activator of NF-kappa B ligand
30 NS (3.8 + 1.7 y.o.) PD (p < 0.01) and E-Cigs (11.5 ± 8.4 pg/mL) GCF than NS.
(RANKL) and osteoprotegerin in
All males CAL (p < 0.01) than NS (3.5 ± 0.7 pg/mL).
the gingival crevicular fluid of CS,
MBL The OPG levels were significantly
WS, E-Cigs, NS
RANKL higher among CS (95.9 ± 7.2 pg/mL)
OPG (p < 0.001) and WS (86.6 ± 5.8 pg/mL)
(p < 0.01) and E-Cigs (77.5 ± 3.4 pg/mL)
(p < 0.05) than NS (21.5 ± 10.7 pg/mL).
There was no significant difference in
RANKL and OPG levels among CS, WS
and E-Cigs.Dent. J. 2022, 10, 103 12 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
At baseline, BOP was significantly
Periodontal and peri-implant
higher in NS than CS and E-Cigs
assessment at baseline and after 3
ALHarthi, 2019 (p < 0.01).
and 6 months of follow-up
[59] In CS, there was no statistically
30 CS (36.4 ± 2.8 y.o.) Scaling
Prospective significant difference in mean PI and PD
28 E-Cigs (32.5 ± 4.8 y.o.) No dental implants GI is worse in CS compared with
To investigate the impact of at 6 months’ follow-up compared with
31 NS (32.6 ± 3.5 y.o.) PI E-Cigs and NS after FMUS
cigarette smoking and vaping on baseline and 3 months follow-up. In
All males BoP
periodontal tissues after a E-Cigs and NS, there was no significant
PD >/= 4 mm
full-mouth ultrasonic scaling difference in PI, BOP, and PD at 3
CAL
months’ (p > 0.05) and 6 months’ (p >
MT
0.05) follow-up.
BOP was significantly higher in NS
compared with CS and E-Cigs (p < 0.01).
Periodontal and peri-implant
PI (p < 0.01), PD (p < 0.01),MMP-9
assessment at baseline
ArRejaie, 2018 (p < 0.001) and IL-1b levels (p < 0.01)
No periodontal treatment
[60] were significantly higher in CS and
Dental implants n. 159 (at least one Higher levels of cytokines in CS and
Case-control 32 CS (40.4 ± 3.5) E-Cigs than NS.
positioned for >= 36 months) E-Cigs suggest greater peri-implant
To compare clinical and 31 E-Cigs (35.8 ± 6.2 y.o.) MBL was significantly higher in CS
PI inflammatory response and so
radiographic peri-implant 32 NS (42.6 ± 2.7 y.o.) compared with E-Cigs and NS
BoP worse clinical and radiographic
parameters and levels of MMP-9 All males (p < 0.01). Significant positive
PD >/= 4 mm peri-implant parameters.
and IL-1b among CS, E-Cigs and associations were found between
MBL
NS MMP-9 (p = 0.0198) and IL-1b (p =
IL-1b
0.0047) levels and MBL in CS; and a
MMP-9
significant positive association between
IL-1b and MBL in E-Cigs (p = 0.0031).Dent. J. 2022, 10, 103 13 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
Periodontal and peri-implant At baseline, there were no differences in
assessment at baseline and after 3 PI, PD, CAL, MBL, and GCF IL-4, IL-9,
months of follow-up IL-10, and IL-13 among E-Cigs and NS.
Scaling and root planing At the 3-month follow-up, there were
Al-Hamoudi, 2020
No dental implants no significant differences in PI, GI, PD,
[61]
PI CAL and MBL in E-Cigs compared to
Cross-sectional
36 E-Cigs (47.7± 5.8 y.o.) GI baseline, while there were significant Levels of GCF IL-4, IL-9, IL-10, and
To investigate the effect of scaling
35NS (46.5 ± 3.4 y.o.) PD reductions in PI, GI, and PD among NS. IL-13 increased after SRP in E-Cigs
and root planing on inflammatory
62M/9F CAL At the 3-month follow-up, GCF IL-4, and NS with CP.
cytokines IL-4, IL-9, IL-10, and
MBL IL-9, IL-10, and IL-13 levels were
IL-13 in E-Cigs and NS with
IL-4 significantly elevated in E-Cigs and in
periodontitis
IL-9 NS (p < 0.05) compared to
IL-10 baseline.After3-month, GCF IL-4, IL-9,
IL-13 IL-10, and IL-13 levels were significantly
Crevicular fluid volume higher in NS (p < 0.05) than in E-Cigs
PI (p < 0.05) and PD (p < 0.05) were
Periodontal and peri-implant significantly higher in CS, WS and
Alqahtani, 2019 assessment at baseline E-Cigs than NS
35 CS (36.3 ± 1.2 y.o.)
[62] No periodontal treatment BoP was higher in NS compared with
33 WS (34.1 ± 1.4 y.o.)
Cross-sectional Dental implants n.137 CS (p < 0.05),WS (p < 0.05) and E-Cigs Nicotine increases the expression of
34 E-Cigs (33.5 ± 0.7 y.o.)
To compare cotinine levels in the PI (p < 0.05). cotinine in the PISF.
35 NS (32.2 ± 0.6 y.o.)
PISF among CS, WS, E-Cigs and PD PISF and cotinine levels were
All males
NS BoP significantly higher among CS (p < 0.05)
Cotinine in the PISF and WS (p < 0.05) and E-Cigs (p < 0.05)
than NS.Dent. J. 2022, 10, 103 14 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
Periodontal and peri-implant
assessment at baseline
No periodontal treatment BOP was significantly higher in NS than
Sinha, 2020 Dental implants n. 66 for E-Cigs and E-Cigs.
[63] 55 for NS PD and PIBL were significantly higher
47 E-Cigs (34.6 ± 6.1 y.o.) E-Cigs show PD, PIBL and TNF-α
Case-control PI in E-Cigs than NS.
45 NS (44.8 ± 2.5 y.o.) levels and IL-1β levels worse than
To evaluate PI, BoP, PD, TNF-α BoP TNF- α levels and IL-1β levels were
All males NS
and IL-1b levels among E-Cigs PD significantly higher in E-Cigs than NS
and NS PIBL PISF concentrations were also found
IL1b relatively higher in E-Cigs than NS.
TNF-a
PISF volume
Periodontal and peri-implant
PI, PD, MMP-8 and TNF-a were higher
assessment at baseline and after 12
in CS and E-Cigs than NS at baseline.
weeks
BOP was higher in NS
Al Deeb, 2020 Photodynamic therapy at baseline +
than other groups.
[64] mechanical debridement (MD)
25 CS (29.5 ± 5.8 y.o.) A statistically significant reduction in PI
Case-control Dental implants n. 111 implants (at PDT with adjunctive mechanical
21 E-Cigs (27.8 ± 3.1 y.o.) and PD parameters was observed on
To assess the effectiveness of least one in service for ≥1.5 years) debridement reduced PI and PD
25 NS (0.2 ± 4.4 y.o.) baseline and at 12 weeks in all groups.
Photodynamic therapy in the PI and cytokines but increased BPO
All males BOP significantly increased in group 1
treatment of peri-implant BoP
and 2 at 12 weeks. A statistically
mucositis in CS, E-Cigs and NS PD
significant reduction from baseline to 12
TNF-a
weeks was reported in the biomarker
MMP-8
levels for all the study groups.
PISF volumeDent. J. 2022, 10, 103 15 of 35
Table 2. Cont.
Periodontal and Peri-Implant
Assessment
Time Points
Authors, Year Population
Treatment
Reference Sample Size
Dental Implants (n.) Main Results Conclusions
Study Design Mean Age
Clinical Parameters
Aim/Objective Gender Ratio
Radiographic Parameters
Crevicular Parameters
Other Parameters
Periodontal and peri-implant
assessment at baseline, after1
month, 6 months and 1 year
BOP and PD increased in all three
AlJasser, 2021 Surgical periodontal treatment
30 CS (46.9 M, 46.6 F y.o.) groups, but CAL uniquely increased in Among the recruited participants,
[65] No dental implants
32 E-Cigs (36 M, 46.8 F y.o.) E-Cigs. CAL after 6 months was
Case-control PD
38 NS (28.6 M, 46.9 F y.o.) CS have higher carbon monoxide and significantly worse only in the
To evaluate the adverse effects of BOP
70M/30F salivary cotinine levels than other E-Cigs
E-Cigs on periodontal health CAL
groups.
Cotinine levels
saliva flow
CO (carbon monoxide)
The PI of 100% of NS changed to ‘00 and
Periodontal and peri-implant
35% change in cigarettes and 30%
assessment at baseline and after 6
change in E-Cigs which is statistically
months
significant (p = 0.016).
Fangxi Xu, 2021 No periodontal treatment
The mean values of PD have shown
[66] 20 CS (54.1 y.o.) Dental implants n. 60
statistically significant change across Vaping was found to be the most
Case-control 20 E-Cigs (46.8 y.o.) PD
the three groups over the four time prevalent risk indicator for
To compare periodontal 20 NS (46.9 y.o.) BOP
intervals of observation. The peri-implantitis.
parameters among CS, E-Cigs and 31M/29F PI
comparison of mean values of IL-1 β,
NS after peri-implantitis treatment IL-1b
IL-6 and TIMP-1 showed statistically
IL-6
significant change across the three
MMP-8
groups over the four intervals of
TIMP-1
observation (p < 0.0001).
Abbreviations: traditional tobacco or cigarette smokers, CS; electronic cigarette or electronic cigarette smokers, E-Cigs; non-smokers, NS; water piper smokers, WP; Years old, y.o.;
Missing data, MD; Plaque index, PI; Bleeding on Probing, BOP; Probing Depth, PD; Clinical Attachment Loss, CAL; MT, number of missing teeth; Marginal Bone Loss (MBL); Community
periodontal index, CPI; Peri-implant bone loss, PIBL; Peri-implant sulcular fluid, PISF; Interleukin, IL; Interferon-gamma, INF-g; Tumor Necrosis Factor-a, TNF-a; Tissue inhibitor
metalloproteinase-1, TIMP-1.Dent. J. 2022, 10, 103 16 of 35
3.3. Data Extraction and Synthesis
Detailed findings related to periodontal clinical and radiographic, as well as inflamma-
tory parameters, are synthesized in Table 3 and in Table 4, respectively; Table 5 describes
peri-implant clinical and radiographic parameters Table 6 reports inflammatory ones.
Table 3. Reported results on clinical and radiographic periodontal and peri-implant parameters.
Author, Year
Periodontal Clinical and
Reference Main Result(s) Considerations
Radiographic Parameter
Study Design
CAL (p < 0.05) was significantly CS and WS have worse CAL
higher among CS and WS values compared to E-Cigs
Mokeem, 2018 [50]
CAL compared to E-Cigs and NS. and NS; E-Cigs and NS have
Case-control
There was no difference in CAL, no significant difference in
between E-Cigs and NS CAL values
CAL (p < 0.05) was significantly
BinShabaib, 2019 [54] higher among CS than NS. No Cigarette smoke negatively
CAL
Case-control differences were among E-Cigs affects the CAL values
and NS
There was no statistically
Vohra, 2020 [55] CS, E-Cigs and NS have
CAL significant difference in CAL,
Case-control similar CAL values
among the CS, E-Cigs and NS
The scores of CAL (p < 0.001) was
significantly higher among CS,
E-Cigs, and NS with periodontitis
Periodontal bacteria
Aldakheel, 2020 [57] compared with NS without
CAL negatively influence
Case-control periodontitis. There was no
CAL values
statistically significant difference
in CAL among CS, E-Cigs, and
NS with periodontitis
At baseline and after 3 months of
Al-Hamoudi, 2020 [61] follow up there were no E-Cigs do not have differences
CAL
Cross-sectional significant differences in CAL with NS for the CAL
between the E-Cigs and NS
ALHarthi, 2018 [59] The levels of CAL remained CAL remains unchanged
CAL
Prospective unchanged in all groups among the groups
There was no statistically
Javed, 2017 [56] significant difference in CAL Smoke does not negatively
CAL
Cohort among individuals among the influence CAL
groups
There were No significant
Karaaslan, 2020 [52] Smoke does not negatively
CAL differences among the groups for
Case-control influence CAL
mean AL
CAL was significantly higher in
Ibraheem, 2020 [58] Smoke negatively affects
CAL CS, WS and E-Cigs compared
Case-control CAL values
with NS
Fangxi Xu, 2021 [66] Vaping negatively affects
CAL CAL increased in E-Cigs
Case-control CAL values
Percentage of sites with BOP were
significantly higher among NS
Mokeem, 2018 [50] compared with CS and WS and
BoP Smoke improves BoP
Case-control E-Cigs. There was no statistically
significant difference in BOP
among CS and WS and E-CigsDent. J. 2022, 10, 103 17 of 35
Table 3. Cont.
Author, Year
Periodontal Clinical and
Reference Main Result(s) Considerations
Radiographic Parameter
Study Design
There was no statistically
Vohra,2020 [55]
BoP significant difference in BOP, Smoke does not influence BoP
Case-control
among the four groups
BOP was significantly higher in
Javed, 2017 [56]
BoP NS than CS (p < 0.01) and E-Cigs Smoke improves BoP
Cohort
(p < 0.01)
There was no statistically
Ibraheem, 2020 [58]
BoP significant difference in BOP Smoke does not improve BoP
Case-control
among individuals in all groups
At baseline, BOP was significantly
higher in NS than CS and E-Cigs
(p < 0.01).
ALHarth, 2018 [59] Cigarette smoke
BoP In E-Cigs and NS, there was no
Prospective improves Bop
significant difference in BOP at 3
months’ (p > 0.05) and 6 months’
(p > 0.05) follow-up
Fangxi Xu, 2021 [66] BoP similarly increased over time
Bop BoP changes in all groups
Case-control in all three groups
BOP was manifested more among
NS than in CS (p < 0.05) and BoP was more often
BinShabaib, 2019 [54]
BoP E-Cigs (p < 0.05). manifested among
Case-control
No differences were among never smokers
E-Cigs and NS
Percentage of sites with plaque
were significantly higher among
CS and WS compared with E-Cigs
(p < 0.05) and NS (p < 0.05).
Mokeem, 2018 [50] Percentage of sites with plaque Smoke increases plaque
PI
Case-control were significantly higher among accumulation.
E-Cigs compared to NS (p < 0.05).
There was no statistically
significant difference in PI among
CS and WS and E-Cigs
PI (p < 0.01) was significantly
Ibraheem, 2020 [58]
PI higher among CS, WS and E-Cigs Smoke gets worse PI
Case-control
than NS
The scores of PI (p < 0.001) were
significantly higher between CS,
E-Cigs, and NS with periodontitis
Aldakheel, 2020 [57] compared with NS without Smoke gets worse
PI
Case-control periodontitis. There was no periodontitis
statistically significant difference
in PI among CS, E-Cigs, and NS
with periodontitis
In CS, there was no statistically
significant difference in mean PI
at 6 months’ follow-up compared
ALHarthi, 2018 [59] with baseline and 3 months’
PI Vaping does not influence PI
Prospective follow-up. In E-Cigs and NS,
there was no significant difference
in PI at 3 months’ (p > 0.05) and 6
months’ (p > 0.05) follow-upDent. J. 2022, 10, 103 18 of 35
Table 3. Cont.
Author, Year
Periodontal Clinical and
Reference Main Result(s) Considerations
Radiographic Parameter
Study Design
PI (p < 0.05), was significantly
BinShabaib, 2019 [54] higher among CS than NS. Smoke gets worse
PI
Case-control No differences were among plaque index
E-Cigs and NS
At baseline, there were no
differences in PI, among E-Cigs
and NS.
Al-Hamoudi, 2020 [61] At the 3-month follow-up, there PI is better among NS after
PI
Cross-sectional were no significant differences in 3-month follow-up
PI, in ES compared to baseline,
while there were significant
reductions in PI, among NS
Vohra, 2020 [55] PD (p < 0.05) was increased in CS Cigarettes smoke gets worse
PI
Case-control than E-Cigs and NS plaque index
Karaaslan, 2020 [52] No significative differences were
PI Smoke does not influence PI
Case-control found between the groups for PI
Vohra, 2020 [55] PD (p < 0.05) was increased in CS Cigarette smoke
PD
Case-control than E-Cigs and NS. gets worse PD
PD ≥ 4 mm (p < 0.01) were
Javed, 2017 [56]
PD significantly higher in CS and in Smoke influences PD
Cohort
E-Cigs compared with NS
PD (p < 0.01) was significantly
Ibraheem, [58]
PD higher among CS, WS, and E-Cigs Smoke gets worse PD
Case-control 2020
than NS
The scores of PD (p < 0.001) were
significantly higher among CS,
E-Cigs, and NS with periodontitis
Aldakheel, 2020 [57] compared with NS without Smoke gets worse
PD
Case-control periodontitis. There was no periodontitis
statistically significant difference
in, PD, among CS, E-Cigs, and NS
with periodontitis.
In CS, there was no statistically
significant difference in PD at 6
months’ follow-up compared with
ALHarthi, 2018 [59]
PD baseline and 3 months’ follow-up. Vaping does not influence PD
Prospective
In E-Cigs and NS, there was no
significant difference in PD at 3
months’ and 6 months’ follow-up
PD (p < 0.05) was significantly
higher among individuals in CS
BinShabaib, 2019 [54]
PD than NS. Smoke gets worse PD
Case-control
No differences were among
E-Cigs and NS
At baseline, there were no
differences in PD, among E-Cigs
and NS.
At the 3-month follow-up, there
Al-amoudi, 2020 [61]
PD were no significant differences in SRP improves PD in NS
Cross-sectional
PD in E-Cigs compared to
baseline values, but there was a
statistically significant reductions
in PD among NSDent. J. 2022, 10, 103 19 of 35
Table 3. Cont.
Author, Year
Periodontal Clinical and
Reference Main Result(s) Considerations
Radiographic Parameter
Study Design
There was no statistically
significant difference in PD
Mokeem, 2018 [50] among E-Cigs c and NS
PD Vaping does not influence PD
Case-control PD was significantly higher
among CS and WS compared
with E-Cigs and NS.
Karaaslan, 2020 [52] No significative differences were
PD Smoke does not influence PD
Case-control found between the groups for PD
Fangxi Xu, 2021 PD similarly increased over time PD increased in all
PD
Case-control in all three groups three groups
At baseline, GI was significantly
higher in NS than E-Cigs; at the
3-month follow-up, there were no
Al-amoudii, 2020 [61] significant differences in GI, in Vaping improves gingival
GI
Cross-sectional E-Cigs compared to baseline, conditions
while there were statistically
significant reductions in GI
among NS.
GI was significantly higher in
Karaaslan, 2020 [52] E-Cigs and EX-CS than CS and GI
GI Smoke improves GI
Case-control was significantly lower in group
E-Cigs than EX-CS
GI (p < 0.001) was significantly
higher among CS, E-Cigs, and NS
with periodontitis compared with
Aldakheel, 2020 [57] GI is worst among subjects
GI NS without periodontitis. There
Case-control with periodontitis
was no statistically significant
difference in GI, among CS,
E-Cigs, and NS with periodontitis
There was no statistically
Vohra, 2020 [55] Smoke does not influence
MBL significant difference in MBL
Case-control MBL among the groups
among CS, E-Cigs and NS
MBL (p < 0.01) was significantly
Ibraheem, 2020 [58]
MBL higher among CS, WS, E-Cigs Smoke gets worse bone loss
Case-control
than NS
The scores mesial (p < 0.001) and
distal (p < 0.001) MBL were
significantly higher among CS,
E-Cigs, and NS with periodontitis
Aldakheel, 2020 [57] compared with NS without Smoke gets worse
MBL
Case-control periodontitis. There was no periodontitis
statistically significant difference
in mesial and distal MBL among
CS, E-Cigs, and NS with
periodontitis
MBL was significantly higher in
CS (p < 0.01) and E-Cigs (p < 0.01)
BinShabaib, 2019 [54]
MBL than NS Smoke gets worse bone loss
Case-control
No differences were among
E-Cigs and NSDent. J. 2022, 10, 103 20 of 35
Table 3. Cont.
Author, Year
Periodontal Clinical and
Reference Main Result(s) Considerations
Radiographic Parameter
Study Design
At baseline, there were no
differences in MBL among E-Cigs
and NS.
Al-Hamoudi, 2020 [61] Vaping does not
MBL At the 3-month follow-up, there
Cross-sectional influence MBL
were no statistically significant
differences in MBL between the
two groups
MBL were significantly higher
among CS and WS compared to
Mokeem, 2018 [50]
MBL E-Cigs and NS Smoke gets worse bone loss
Case-control
There was no difference in MBL
among E-Cigs and NS
Javed, 2017 [56] There was no difference in MBL No differences
MBL
Cohort among the groups among the groups
Javed, 2017 [56] There was no difference in MT
MT Smoke does not influence MT
Cohort among the groups
There was no statistically
Vohra, 2020 [55]
MT significant difference in MT Smoke does not influence MT
Case-control
among CS, E-Cigs, NS
ALHarthi, 2018 [59] There was no difference in the
MT Smoke does not influence MT
Prospective numbers of MT in all groups
BinShabaib, 2019 [54]
MT No differences among the groups Smoke does not influence MT
Case-control
Table 4. Reported results on crevicular inflammatory periodontal parameters.
Author, Year
Periodontal Inflammatory
Reference Main Result(s) Considerations
Parameter
Study Design
There was no difference in
IL-1β levels among E-Cigs
Cigarette and pipe smoke
Mokeem, 2018 [50] and NS
IL-1b increase gingival
Case-control IL-1β (p < 0.01) levels were
inflammation
significantly higher among CS,
WS than E-Cigs and NS
The concentration of IL-1β
was significantly higher in the
BinShabaib, 2019 [54] GCF samples of CS (p < 0.05) Cigarettes smoke increase
IL-1b
Case-control than E-Cigs and NS. No inflammation
differences were among
E-Cigs and NS
The concentration of IL-6 was
significantly higher in the
Bin Shabaib, 2019 [54] GCF samples of CS (p < 0.05) Cigarettes smoke increase
IL-6
Case-control than E-Cigs and NS. No inflammation
differences were among
E-Cigs and NS
IL-6 (p < 0.01) levels were
Mokeem, 2018 [50] Cigarette smoke increases
IL-6 significantly higher among CS,
Case-control gingival inflammation
WS than E-Cigs and NSDent. J. 2022, 10, 103 21 of 35
Table 4. Cont.
Author, Year
Periodontal Inflammatory
Reference Main Result(s) Considerations
Parameter
Study Design
The concentration of TNF-α
was significantly higher in the
GCF samples of CS (p < 0.05) Cigarettes smoke increase
TNF-a Bin Shabaib,2019 [54]
than E-Cigs and NS. No inflammation
differences were among
E-Cigs and NS
TNF-a level of Group CS
Karaaslan, 2020 [52] (4.20 +/− 0.14) was Smoke increases gingival
TNF-a
Case-control significantly higher than inflammation
E-Cigs
Cotinine levels were
Mokeem, 2018 [50] significantly higher among CS Smoke increases gingival
COTININE
Case-control (p < 0.001) and WS (p < 0.001) inflammation
and E-Cigs (p < 0.001) than NS
Fangxi Xu, 2021 [66] Salivary cotinine levels was CS have highest salivary
COTININE
Case-control highest among CS cotinine levels
IL-8 level of CS
Karaslaan, 2020 [52] (70.47 +/− 2.76) was
IL-8 Smoke improves il-8 levels
Case-control significantly lower than in
E-Cigs and FS
The concentrations of MMP-8
were significantly higher in
BinShabaib, 2019 [54] the GCF samples of CS Cigarettes smoke increase
MMP-8
Case-control (p < 0.05) than E-Cigs and NS. inflammation
No differences were among
E-Cigs and NS
The concentration of I FN-γ
was significantly higher in the
BinShabaib, 2019 [54] GCF samples of CS (p < 0.05) Cigarettes smoke increase
IFN-y
Case-control than ES and NS. No inflammation
differences were among
E-Cigs and NS
E-Cigs and CS were each
significantly associated with
Periodontal disease was more
increased periodontal disease
CPI Jeong, 2020 [26] prevalent in E-Cigs and CS
rates. This study suggests that
than NS
vaping may not be a safe
alternative to smoking
At baseline, there were no
differences, and GCF IL-4
among E-Cigs and NS.
Levels of GCF IL-4 increased
At the 3-month follow-up,
after SRP in E-Cigs and NS
GCF IL-4 levels were
Al-Hamoudi, 2020 [61] with CP; however, the
IL-4 significantly elevated in ES
Cross-sectional anti-inflammatory effect of
and in NS (p < 0.05) compared
SRP was more profound in NS
to baseline. After3-month,
than in E-Cigs
GCF IL-4, levels were
significantly higher in NS
(p < 0.05) than in E-CigsDent. J. 2022, 10, 103 22 of 35
Table 4. Cont.
Author, Year
Periodontal Inflammatory
Reference Main Result(s) Considerations
Parameter
Study Design
At baseline, there were no
differences in IL-9, among
E-Cigs and NS.
Levels of GCF IL-9 increased
At the 3-month follow-up,
after SRP in E-Cigs and NS
GCF IL-9 levels were
Al-Hamoudi, 2020 [61] with CP; however, the
IL-9 significantly elevated in
Cross-sectional anti-inflammatory effect of
E-Cigs and in NS (p < 0.05)
SRP was more profound in NS
compared to baseline. After 3
than in E-Cigs
months, GCF IL-9 levels were
significantly higher in NS
(p < 0.05) than in E-Cigs
At baseline, there were no
differences in IL-10 among
E-Cigs and NS.
Levels of GCF IL-10 increased
At the 3-month follow-up,
after SRP in E-Cigs and NS
GCFIL-10 levels were
Al-Hamoudi, 2020 [61] with CP; however, the
IL-10 significantly elevated in
Cross-sectional anti-inflammatory effect of
E-Cigs and in NS (p < 0.05)
SRP was more profound in NS
compared to
than in E-Cigs
baseline.After3-month, GCF
IL-10, was significantly higher
in NS (p < 0.05) than in E-Cigs
At baseline, there were no
differences in IL-13 among
E-Cigs and NS.
Levels of GCF IL-13 increased
At the 3-month follow-up, GCF
after SRP in E-Cigs and NS
IL-13 levels were significantly
Al-Hamoudi, 2020 [61] with CP; however, the
IL-13 elevated in E-Cigs and in NS
Cross-sectional anti-inflammatory effect of
(p < 0.05) compared to
SRP was more profound in NS
baseline.After3-month, GCF
than in E-Cigs
IL-13 levels were significantly
higher in NS (p < 0.05) than in
E-Cigs
Fangxi Xu, 2021 [66] CO levels was highest
CO CS have highest CO levels
Case-control among CS
Although the GSH-Px level of
Group II was higher than
Group I, this difference was
CS and E-Cigs had the same
not statistically significant, but
Karaaslan, 2020 [52] unfavorable effects on the
GSH-PX AND 8-OHdG the mean GSH-Px level of
Case-control markers of oxidative stress
Group III was significantly
and inflammatory cytokines
higher than in Groups I and II.
There was no significant
association among the groups
The RANKL levels were
significantly higher among CS
(14.9 ± 8.2 pg/mL) (p < 0.001)
and WS (12.6 ± 8.8 pg/mL) CS and WS and E-Cigs are
Ibraheem, 2020 [58] (p < 0.01) and E-Cigs associated with an
RANKL
Case-control (11.5 ± 8.4 pg/mL) (p < 0.01) increased expression of
than NS (3.5 ± 0.7 pg/mL). RANKL in the GCF
There was no significant
difference in RANKL among
CS, WS and ESDent. J. 2022, 10, 103 23 of 35
Table 4. Cont.
Author, Year
Periodontal Inflammatory
Reference Main Result(s) Considerations
Parameter
Study Design
The OPG levels were
significantly higher among CS
(95.9 ± 7.2 pg/mL) (p < 0.001) CS and WS and E-Cigs are
Ibraheem, 2020 [58]
OPG and WS (86.6 ± 5.8 pg/mL) associated with an increased
Case-control
(p < 0.01) and E-Cigs expression of OPG in the GCF
(77.5 ± 3.4 pg/mL) (p < 0.05)
than NS (21.5 ± 10.7 pg/mL)
Table 5. Reported results on clinical and radiographic peri-implant parameters.
Author, Year
Clinical and Radiographic
Reference Main Result(s) Considerations
Peri-Implant Parameters
Study Design
Peri-implant BOP was
ArRejaie, 2018 [60] significantly higher in NS
BoP Smoke improves Bop
Case-control compared with CS and E-Cigs
(p < 0.01)
BOP was statistically
Al-Aali, 2018 [51]
BoP significantly higher in NS Vaping smoke improves Bop
Case-control
compared to E-Cigs (p < 0.01)
Sinha, 2020 [63] BOP was significantly higher
BoP Vaping smoke improves Bop
Case-control in NS than E-Cigs
BoP was higher in NS
Alqahtani, 2019 [62] compared with CS (p < 0.05),
BoP Smoke improves Bop
Cross-sectional WS (p < 0.05) and E-Cigs
(p < 0.05)
BOP was statistically
Al Deeb, 2020 [64]
BoP significantly higher in NS Smoke improves Bop
Case-control
than other groups
BOP in CS, WS, and E-Cigs
Alqahtani, 2019 [62]
BoP showed statistical differences Smoke improves Bop
Cross-sectional
(p < 0.01) respect to NS
BOP was statistically
Al-Aali, 2018 [51]
BoP significantly higher in NS Vaping smoke improves Bop
Case-control
compared to E-Cigs (p < 0.01)
The prevalence of BOP was
observed in the three groups
BoP AlJasser, 2021 [65] Smoke improves Bop
as 72%, (CS) 76.5% (E-Cigs)
and 88.9% (NS) at baseline
PI was significantly higher
among individuals CS
Alqahtani, 2019 [62] Smoke gets worse
PI (p < 0.05), WS (p < 0.05), and
Cross-sectional plaque index
E-Cigs (p < 0.05) compared
with NS
PI (p < 0.01 was significantly
higher in CS and
ArRejaie, 2018 [60] E-Cigs than NS. Cigarettes smoke gets worse
PI
Case-control There were differences plaque index
statistically significantly
among CS and E-CigsDent. J. 2022, 10, 103 24 of 35
Table 5. Cont.
Author, Year
Clinical and Radiographic
Reference Main Result(s) Considerations
Peri-Implant Parameters
Study Design
PI showed no significant
Al-Aali, 2018 [51]
PI difference between NS and Vaping does not influence PI
Case-control
E-Cigs
PI showed no significant
Sinha, 2020 [63]
PI difference between NS and Vaping does not influence PI
Case-control
E-Cigs
PI (p < 0.05) was significantly
Alqahtani, 2019 [62] Smoke gets worse
PI higher in CS, WS and E-Cigs
Cross-sectional plaque index
than NS
PI was higher in CS and
E-Cigs than NS at baseline.
Al Deeb, 2020 [64] Statistically significant Smoke gets worse plaque
PI
Case-control reduction in PI was observed index
on baseline and at 12 weeks in
all groups
PI of 100% of NS had changed
to ‘00 and 35% change in
AlJasser, 2021 [65] PI was higher in NS than
PI cigarettes and 30% change in
Case-control other groups
E-Cigs which is statistically
significant (P = 0.016)
ArRejaie, 2018 [60] PD was significantly higher in
PD Smoke gets worse PD
Case-control CS and E-Cigs than NS
PD was statistically
Al-Aali, 2018 [51]
PD significantly higher in E-Cigs Vaping gets worse PD
Case-control
than NS
Sinha, 2020 [63] PD was significantly higher in
PD Vaping gets worse PD
Case-control E-Cigs than NS
PD was significantly higher
among CS, WS and E-Cigs
Alqahtani, 2019 [62] compared with NS.
PD Smoke gets worse PD
Cross-sectional Among smokers, CS and WS
showed significantly higher
PD compared with E-Cigs
PD (p < 0.05) was significantly
Alqahtani, 2019 [62]
PD higher in CS, WS and E-Cigs Smoke gets worse PD
Cross-sectional
than NS
PD was higher in CS and
E-Cigs than NS at baseline.
Al Deeb, 2020 [64] Statistically significant
PD Smoke gets worse PD
Case-control reduction in PD parameter
was observed on baseline and
at 12 weeks in all groups
PD have shown statistically
significant change across the
AlJasser, 2021 [65]
PD three groups over the Smoke gets worse PD
Case-control
four-time intervals of
observation (P = 0.024)Dent. J. 2022, 10, 103 25 of 35
Table 5. Cont.
Author, Year
Clinical and Radiographic
Reference Main Result(s) Considerations
Peri-Implant Parameters
Study Design
Peri-implant bone loss was
Al-Aali, 2018 [51] Smoke increases periodontal
MBL statistically significantly
Case-control inflammation
higher in E-Cigs than NS
MBL was significantly higher
in CS compared with E-Cigs
ArRejaie, 2018 [60] and NS (p < 0.01). Cigarettes smoke gets worse
MBL
Case-control There were differences bone loss
statistically significantly
among CS and E-Cigs
Sinha, 2020 [63] MBL was significantly higher
MBL smoke gets worse bone loss
Case-control in E-Cigs than NS
MBL (p < 0.01) was
significantly higher among CS,
WS and E-Cigs compared
Alqahtani, 2019 [62] with NS. Cigarettes smoke gets worse
MBL
Cross-sectional CS and WS showed bone loss
significantly higher
Peri-implant BL compared
with E-Cigs (p < 0.05)
ArRejaie, 2018 [60] PD was significantly higher in
PD Smoke gets worse PD
Case-control CS and E-Cigs than NS
Table 6. Reported results on crevicular inflammatory peri-implant parameters.
Author, Year
Inflammatory Periodontal
Reference Main Result(s) Considerations
Parameter
Study Design
IL-1 b levels were statistically
significantly higher in CS than
ArRejaie, 2018 [60] E-Cigs and NS
IL-1 b Smoke increase inflammation
Case-control IL-1-b levels were statistically
significantly higher in E-Cigs
than NS
IL-1β was significantly higher
in CS, WS, and
Alqahtani, 2019 [62] E-Cigs than NS. Smoke increases gingival
IL-1 b
Cross-sectional No statistical differences for inflammation
cytokines were observed
between CS and WS
IL-1b (p < 0.01) was
Al-Aali, 2018 [51] Smoke increases gingival
IL-1 b statistically significantly
Case-control inflammation
higher in E-Cigs than NS
Sinha, 2020 [63] IL-1 b levels was significantly Smoke increases gingival
IL-1 b
Case-control higher in E-Cigs than NS inflammation
Comparison of mean IL-1β
values showed statistically
AlJasser, 2021 [65] significant variation between
IL-1 b Smoke increases inflammation
Case-control the three groups in the four
observation intervals
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