| |

Received: 12 November 2018    Revised: 15 December 2018    Accepted: 20 December 2018

DOI: 10.1111/jicd.12403

REVIEW ARTICLE
Oral and Maxillofacial Surgery

Effect of waterpipe smoking on peri-­implant health: A

systematic review and meta-­analysis

Zohaib Akram1  | Fawad Javed2 | Fahim Vohra3

1
Department of Oral Restorative and
Rehabilitative Sciences, The University of Abstract
Western Australia, Perth, Western Australia, The aim of the present review was to evaluate the effect of waterpipe smoking (WS)
Australia
2 on clinical peri-­implant inflammatory parameters compared to non-­smokers (NS) with
Department of Periodontology, Stony
Brook University, Stony Brook, New York dental implants. Literature searches were performed using bibliographic databases
3
Department of Prosthetic Dental up to May 2018. Primary outcomes included peri-­implant bone loss (PIBL), while sec-
Sciences, King Saud University, Riyadh,
Saudi Arabia
ondary outcomes were probing depth (PD), plaque index, and bleeding on probing.
Relative risk (RR) and 95% confidence intervals (CI) for each PIBL and PD were esti-
Correspondence
Dr Zohaib Akram, Department of Oral
mated by a random-­effect model. Four retrospective case-­control studies were in-
Restorative and Rehabilitative Sciences, The cluded in the qualitative and quantitative syntheses. All of the included studies
University of Western Australia, Perth, WA,
Australia.
showed statistically-­significantly worse peri-­implant outcomes in WS compared to
Email: drzohaibakram@gmail.com NS. Considering the effects of WS on peri-­implant parameters, significant heteroge-
neity for PIBL (Q-­value = 34.21, P < 0.0001, I2 = 94.16%) and PD (Q-­value = 51.97,
P < 0.0001, I2 = 96.15%) was observed between both groups. The overall RR for PIBL
(RR = 3.32, 95% CI = 1.01-­3.97, P = 0.001) and PD (RR = 3.40, 95% CI = 1.91-­7.17,
P = 0.001) were significant between WS and NS groups. WS has detrimental effect
on peri-­implant health. Clinicians should instruct and advise patients about poor
prognosis and peri-­implant diseases caused by WS.

KEYWORDS
bleeding on probing, crestal bone loss, meta-analysis, peri-implantitis, waterpipe

1 |  I NTRO D U C TI O N
It has been well established that habitual cigarette smoking is a
threat for soft tissue inflammation and marginal bone destruction
around natural dentition and osseointegrated dental implants. 1,2
It has also been documented that tooth loss (as a consequence of
periodontitis) and implant failure (as a result of peri-­implantitis) are
more often observed in cigarette smokers than non-­smokers (NS).3,4
A different smoking habit that stemmed from Middle Eastern coun-
tries (ie, Egypt, Saudi Arabia, Qatar, and the United Arab Emirates)
and is practiced in many Western countries (including the USA and
the UK) and many other Eastern European countries (ie, Latvia and
Slovakia) is waterpipe smoking (WS), also known as narghile, hookah,
and shisha.5-7 A typical misconception among waterpipe smokers is
that this kind of tobacco inhalation does not produce harmful ef-
fects on health as produced by usual cigarette smoking, because the
smoke is filtered through water that absorbs lethal substances prior
to the inhalation of smoke.8 However, clinical reports have demon-
strated that oral disorders (ie, periodontal diseases and oral cancer)
and respiratory and cardiovascular diseases are more often reported
among waterpipe smokers than NS.1,9,10
In a recent clinical retrospective study, Javed et al indicated that
periodontal inflammation is worse in waterpipe smokers compared
with NS.1 They demonstrated that WS is as hazardous to periodon-
tal health as conventional cigarette smoking.1 Likewise, studies have
also shown that cigarette smoking retards bone healing around den-
tal implants and significantly increases the risk of peri-­implant bone
loss (PIBL).11,12

J Invest Clin Dent. 2019;10:e12403. wileyonlinelibrary.com/journal/jicd © 2019 John Wiley & Sons Australia, Ltd  |  1 of 7
https://doi.org/10.1111/jicd.12403
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2 of 7       AKRAM et al.
Recent investigations have evaluated the effect of WS on peri-­
implant parameters and have shown relatively worse peri-­implant
outcomes in those who have been smoking for approximately
1 year.13,14
The present meta-­a nalysis was conducted in order to provide
clinicians with a quantified outline of the available data on the
relative influence of WS on peri-­implant inflammatory and clin-
ical parameters. Therefore, the goal of the present systematic
review and meta-­a nalysis was to formulate and answer the fol-
lowing PECO ‘population; exposure; comparison, and outcome’
focus question: In participants with dental implants (popula-
tion), what is the impact/effect of waterpipe smoking (exposure)
in comparison to NS (comparison) on peri-­implant bone level
(outcome)?
2 |  M ATE R I A L S A N D M E TH O DS
2.1 | Review registration and protocol guidelines
The record for the present review was published at the National
Institute for Health Research PROSPERO,15 International
Prospective Register of Systematic Reviews website (http://www.
crd.york.ac.uk/PROSPERO) (registration no. CRD42018095256).
A protocol was formulated that adhered to the guidelines of the
Preferred Reporting Items for Systematic Review and Meta-­Analysis
(PRISMA) statement. 16
2.2 | Eligibility criteria for this review according to
population, exposure, comparison, and outcome
The studies used for the present review were case control, cross-­
sectional, and retrospective studies that included at least 10 partici-
pants per group with osseointegrated dental implants in either jaw
(population). These studies compared WS with NS (exposure). PIBL
was described as the primary outcome, whereas peri-­implant prob-
ing depth (PD) was described as the secondary outcome measure
(outcome).
In order to report the aim of the present study broadly, clinical
parameters, such as PIBL and PD in millimeters, were further ad-
dressed. Studies were excluded if the primary outcome (PIBL) was
missing. Only literature published in the English language was used
for the present systematic review. Animal experimentation stud-
ies, letters to the editor, abstracts, review articles, and unpublished
studies were excluded.
2.3 | Information sources
Literature searches were conducted by two independent reviewers
using four different bibliographic databases (Medline: 1974-­May
2018, EMBASE: 1994-­May 2018, Cochrane Central Register of
Controlled Trials: 1998-­May 2018, and Cochrane Oral Health Group
Trials Register: 1997-­May 2018) for articles focusing on the aim of
the study and PECO question.
2.4 | Search strategy and search terms
Combinations of MeSH terms and free-­text words with Boolean
operators were used: waterpipe (MeSH terms) OR narghile OR
hookah OR shisha AND peri-­implant OR peri-­implant disease OR
peri-­implantitis AND plaque index OR plaque scores OR bleeding OR
bleeding on probing OR probing depth OR bone loss OR marginal
bone loss OR crestal bone loss OR dental implants OR osseointe-
grated dental implants.
2.5 | Study selection
Independent screening of the main titles and abstracts for eligible
papers was conducted by two reviewers. The reviewers performed
a thorough examination of the titles and abstract for possible eligi-
bility of full-­text reviewing. The reviewers then selected articles for
full-­text screening. In addition, a manual search of peer-­reviewed
ISI-­indexed journals (Clinical Implant Dentistry and Related Research,
Journal of Periodontology, Journal of Clinical Periodontology, and
Journal of Periodontal Research) for pertinent articles was per-
formed. The inter-­search agreement between the two reviewers
was computed in SPSS (SPSS, Chicago, IL, USA) using Cohen's
kappa test. Eligible articles that satisfied the selection standard
were processed for data extraction. In order to reduce risk of bias
on the screening stage and to offer high level of evidence, the out-
line for the present study adhered to the PRISMA guidelines.16
2.6 | Data extraction
The data from the included studies was charted according to the study
design, patient demographics (which included sample size and mean
age in years), sex distribution, potential covariates, study groups, WS
(duration, daily frequency, and duration of smoking session), peri-­
implant parameters, main results, and source of funding from the in-
cluded studies. Data collected were based on the focused question.
Disagreements between reviewers were resolved through discussion.
2.7 | Risk of bias in individual studies
The assessment of risk of bias across included studies was per-
formed by two assessors based on a grading system developed by
the Newcastle Ottawa Scale (NOS).17 This quality assessment uses
a star system to assess the studies on three broad perspectives:
the selection of the study groups (4 stars), the comparability of the
groups (2 stars), and the ascertainment of either the exposure or
outcome of interest (3 stars).17
2.8 | Quantitative analysis
In the present review, the primary outcome was PIBL in millime-
ters, whereas the secondary outcome was peri-implant PD. Meta-­
analyses were conducted separately for each of the primary and
secondary outcome (PD). In addition, heterogeneity for PIBL and PD
AKRAM et al.
was assessed using χ2-­test and I2 test. A random-­effects model was
2
employed if the test revealed substantial heterogeneity (I  > 50%).
Otherwise, if non-­significant (I2 ≤ 50%), a fixed-­effects model was
used.18 Forest plots were generated to graphically represent relative
risk (RR) and 95% confidence intervals (CI). Level of significance for
both heterogeneity and pooled effect was adjusted at P < 0.05.
3 | R E S U LT S
3.1 | Article selection
The search produced 148 titles and abstracts at the initial step. All
articles were scanned for duplication and removed if duplicated
(N = 13); 123 articles were excluded, as they were found unsuit-
able to the PECO question (ĸ score: 0.85 [0.78-­0.92]). Twelve pa-
pers were selected for full-­text reading. Of these, eight studies
were further excluded. After the final stage of selection, four stud-
ies were included and processed for data extraction (ĸ score: 0.97
[0.94-­1.00]).13,14,19,20 All studies were performed at university hos-
pitals.13,14,19,20 The PRISMA flowchart of the search process is pre-
sented in Figure 1, with reasons of exclusion indicated.16
3.2 | General description of included studies
All clinical studies were retrospective case-­control studies.13,14,19,20
Three studies were performed in Saudi Arabia,14,19,20 and one study in
Pakistan.13 In all studies, the number of participants ranged between
40 and 84, with the mean age between 43.4 and 51.2 years.13,14,19,20
None of the studies included female participants. In total, 129 water-
13,14,19,20
pipe smokers and 128 NS were included in all studies. All but
14
one of the included studies excluded potentially confounding factors ;
F I G U R E   1   Preferred Reporting Items for Systematic Review and Meta-­Analysis flow diagram for studies retrieved through the search
and selection process
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      3 of 7
the study that did not exclude potentially cofounding factors included
diabetic participants. The duration of WS ranged between 16.2 and
21.5 years, whereas daily frequency ranged from four to five times
daily in the included studies.13,14,19,20 The duration of WS sessions
was approximately 35 minutes daily. Three studies reported university
funding (Table 1).14,19,20
3.3 | Results of the risk of bias assessment
Study quality, as assessed by the NOS, varied considerably across
the studies, ranging from 4/9 to 5/9. The quality assessment of the
accepted studies is presented in Table 2. All of the included articles
were of moderate quality.13,14,19,20
3.4 | Clinical peri-­implant inflammatory
parameters of included studies
The results for primary (PIBL) and secondary outcomes (PD) are pre-
sented in Table 1. Only one study reported PIBL as mesial and distal
measurements. For PD, only one study reported measurements as
≥4 mm. All of the accepted studies reported mean PIBL and PD which
ranged from 5.6 to 5.8 mm and 6.7 to 6.9 mm respectively.13,14,19,20
3.5 | Main outcomes of the accepted studies
All studies reported that WS showed significantly worse peri-­implant
parameters compared to non-­smokers.13,14,19,20 For quantitative syn-
thesis, a meta-­analysis was performed. Three studies presented data
to be included in the meta-­analysis considering the effects of WS on
PIBL and PD.13,14,20 Significant heterogeneity was observed for both
PIBL and PD; therefore, a random-­effects model was employed.
TA B L E   1   General description of the included studies

Smoking duration;
|

Sample size; Systemic daily frequency;

4 of 7      

Study design and mean age (y); conditions/ duration of smoking

Investigators setting females (%) covariates Study groups (N) session Peri-­implant parameters Study outcome Funding source
Abduljabbar Retrospective 66; Excluded 33 WS 16.2 y; 5.3 times Probing depth (mm) Waterpipe smokers showed University
et al20 case control; WS: 48.6 33 NS daily; 35.6 min WS: 6.7 ± 0.4 significantly worse peri-­ funding
Saudi Arabia; NS: 51.2; 0% NS: 4.6 ± 0.3 implant parameters compared
university clinic Peri-­implant bone loss (mm) to non-­smokers (P < 0.001)
WS: 5.8 ± 1.2
NS: 4.4 ± 0.3
Al-­Sowygh et al14 Retrospective 40; Included (type 21 WS 18.5 y; 5.5 times Plaque index (%) Waterpipe smokers showed University
case control; WS: 43.4 2 diabetes 19 NS daily; 33.5 min WS: 36.5 ± 5.2 significantly worse peri-­ funding
Saudi Arabia; NS: 45.3; 0% mellitus) NS: 22.2 ± 4.8 implant parameters compared
university clinic Bleeding on probing (%) to non-­smokers (P < 0.05)
WS: 8.6 ± 3.5
NS: 32.5 ± 4.8
Probing depth (% ≥4 mm)
WS: 15.3 ± 1.8
NS: 4.8 ± 0.6
Peri-­implant bone loss (mm)
WS:
Mesial: 2.5 ± 0.2
Distal: 2.7 ± 0.1
NS:
Mesial: 0.6 ± 0.4
Distal: 0.8 ± 0.3
Al-­Sowygh et al19 Retrospective 66; Excluded 33 WS 16.2 y; 5.3 times Probing depth (mm) Waterpipe smokers showed University
case control; WS: 48.6 33 NS daily; 35.6 min WS: 6.7 ± 0.4 significantly worse peri-­ funding
Saudi Arabia; NS: 51.2; 0% NS: 4.6 ± 0.3 implant parameters compared
university clinic Peri-­implant bone loss (mm) to non-­smokers (P < 0.001)
WS: 5.8 ± 1.2
NS: 4.4 ± 0.3
ALHarthi et al13 Retrospective 84; Excluded 42 WS 21.5 y; 4.5 times Plaque index (%) Waterpipe smokers showed Not stated
case control; WS: 44.5 43 NS daily; 24.2 min WS: 57.3 ± 3.4 significantly worse peri-­
Pakistan; NS: 46.6; 0% NS: 39.1 ± 4.5 implant parameters compared
university clinic Bleeding on probing (%) to non-­smokers (P < 0.01)
WS: 20.4 ± 2.4
NS: 41.5 ± 2.7
Probing depth (mm)
WS: 6.9 ± 1.1
NS: 5.1 ± 0.2
Peri-­implant bone loss (mm)
WS: 5.6 ± 0.4
NS: 4.1 ± 0.3
AKRAM et al.

NS, non-­smokers; WS, waterpipe smoking.

AKRAM et al.
TA B L E   2   Evaluation of the risk of bias
Authors
using the Newcastle-­Ottawa Scale
20
Abduljabbar et al
Al-­Sowygh et al14
19
Al-­Sowygh et al
ALHarthi et al13
F I G U R E   2   Forest plot showing (A) peri-­implant bone loss and (B) probing depth between waterpipe smokers and non-­smokers. CI,
confidence interval; NS, non-­smokers; WS, waterpipe smoking
Considering the effects of WS on peri-­implant parameters, significant
heterogeneity for PIBL (Q-­value = 34.21, P < 0.0001, I2 = 94.16%) and PD
(Q-­value = 51.97, P < 0.0001, I2 = 96.15%) was noticed among both groups
in the included studies. The overall RR for PIBL (RR = 3.32, 95% CI = 1.01-­
3.97, P = 0.001) (Figure 2A) and PD (RR = 3.40, 95% CI = 0.91-­7.17,
P = 0.001) (Figure 2B) were significant between the WS and NS groups.
4 |  D I S CU S S I O N
The current study was based on the hypothesis that WS has worse
clinical peri-­implant inflammatory parameters compared to NS with
dental implants. All retrospective case-­control studies included in
the present systematic review backed the aforementioned hypoth-
esis. To the best of our knowledge, the present review is the first
to provide clinicians with a quantified summary of the available evi-
dence on the relative influence of WS on clinical and radiographic
peri-­implant inflammatory parameters.
The pathological mechanism for worse peri-­implant outcomes in
WS can be corroborated with mechanisms that are involved in cig-
arette smoking. Smoke from waterpipes contain harmful chemicals,
|
      5 of 7
Selection Comparability Exposure Score Quality
☆☆ ☆ ☆ 4 Moderate
☆☆☆ ☆ ☆ 5 Moderate
☆☆☆ ☆ ☆ 5 Moderate
☆☆ ☆ ☆ 4 Moderate
such as CO, nicotine, and tar. 21-23 These toxins remain in smokers
for long durations. Research indicates that nicotine escalates the
expression of pro-­inflammatory cytokines (ie, interleukin-­1β and
tumor necrosis factor-­α), which play a significant role in enhancing
alveolar bone loss around natural teeth. 24 Raised levels of these pro-­
inflammatory cytokines have also been identified in the peri-­implant
sulcular fluid of patients with peri-­implantitis. 2,25 Furthermore, re-
sults from a recent meta-­analysis reported that nicotine from to-
bacco smoke impairs new bone formation around osseointegrated
implants and bone-­to-­implant contact. 26 Moreover, nicotine has also
been shown to suppress cellular healing response and increase the
accumulation of the oral biofilm (a potential risk factor that could
led to peri-­implantitis) in smokers. 27 These mechanisms might sug-
gest possible reasons for peri-­implant destruction among waterpipe
smokers.
The assessment of bleeding on probing (BOP) is a classical in-
dicator of both periodontal and peri-­implant soft tissue inflam-
mation. 28,29 However, tobacco smokers might be unaware of the
possible constant oral soft tissue inflammatory process, as they
demonstrate less sites with BOP compared with NS.30 In the pres-
ent review, the data from the studies included showed a percentage
 |
6 of 7       AKRAM et al.
of peri-­implant sites that presented BOP were significantly higher
among NS as compared to waterpipe smokers. It has been suggested
that nicotine exerts a vasoconstrictive effect on gingival blood flow,
which reduces gingival bleeding in tobacco smokers compared with
NS.31,32 The findings of the present review suggest, and therefore
disagree, with the general insight that WS is less hazardous than cig-
arette smoking, as water in waterpipes sieves chemicals, including
8
nicotine.
The meta-­analysis showed significant heterogeneity for PIBL and
PD among the WS and NS groups. This possibly could be due to the in-
clusion of patients with different case definitions of peri-­implantitis at
the recruitment stage. None of the studies included case definitions, as
proposed by the consensus report of the Eighth European Workshop
on Periodontology.33 Two of the studies included were from the same
study groups that might have produced a bias.14,19 Although calibra-
tion was performed for clinical peri-­implant assessment, the precision
of measurements was not calibrated in PIBL, which could add to the
geometric errors on the digital radiographs in the included studies. The
small number of accepted studies might add another limitation, which
could have an overall impact on the weight of the study. Moreover, the
search process included articles only in English, which might also have
resulted in publication bias, with potentially relevant studies published
in other languages being excluded.34 All of these factors might have
caused discrepancies, which make interpretations difficult, and such
findings should be accepted with caution.
Within these limits, individuals utilizing WS could be at risk of
worse peri-­implant tissue inflammation. Clinicians and implantolo-
gists should counsel and teach young and middle-­aged adults about
the association of peri-­implant destruction and detrimental effects
of WS, and provide frequent education to such cohorts to desist
from waterpipe inhalation. In addition, community health-­awareness
programs should be undertaken, and anti-­tobacco companies should
regularly and consistently instruct the general population about the
hazardous effects of tobacco smoking use on peri-­implant and gen-
eral health.
4.1 | Conclusion
Waterpipe smoking has a detrimental effect on peri-­implant health.
Clinicians should educate and warn patients about poor prognosis
and peri-­implant diseases caused by WS.
ORCID
Zohaib Akram  https://orcid.org/0000-0001-9618-8818
REFERENCES
1. Javed F, Al-Kheraif AA, Rahman I, et al. Comparison of clinical and
radiographic periodontal status between habitual water-­pipe smok-
ers and cigarette smokers. J Periodontol. 2016;87:142‐147.
2. Akram Z, Vohra F, Bukhari IA, Sheikh SA, Javed F. Clinical and ra-
diographic peri-­implant parameters and proinflammatory cytokine
levels among cigarette smokers, smokeless tobacco users, and non-
tobacco users. Clin Implant Dent Relat Res. 2018;20:76‐81.
3. Dietrich T, Walter C, Oluwagbemigun K, et  al. Smoking, smoking
cessation, and risk of tooth loss: the EPIC-­Potsdam study. J Dent
Res. 2015;94:1369‐1375.
4. Chrcanovic BR, Kisch J, Albrektsson T, Wennerberg A. Factors influ-
encing early dental implant failures. J Dent Res. 2016;95:995‐1002.
5. Akl EA, Ward KD, Bteddini D, et  al. The allure of the waterpipe:
a narrative review of factors affecting the epidemic rise in wa-
terpipe smoking among young persons globally. Tob Control.
2015;24:i13‐i21.
6. Jawad M, Lee JT, Millett C. Waterpipe tobacco smoking prevalence
and correlates in 25 Eastern Mediterranean and Eastern European
countries: cross-­sectional analysis of the Global Youth Tobacco
Survey. Nicotine Tob Res. 2015;18:395‐402.
7. Jawad M, Charide R, Waziry R, Darzi A, Ballout RA, Akl EA. The
prevalence and trends of waterpipe tobacco smoking: a systematic
review. PLoS ONE. 2018;13:e0192191.
8. Husain H, Al-Fadhli F, Al-Olaimi F, et  al. Is smoking shisha safer
than cigarettes: comparison of health effects of shisha and ciga-
rette smoking among young adults in Kuwait. Med Princ Pract.
2016;25:117‐122.
9. Montazeri Z, Nyiraneza C, El-Katerji H, Little J. Waterpipe smok-
ing and cancer: systematic review and meta-­analysis. Tob Control.
2017;26:92‐97.
10. Waziry R, Jawad M, Ballout RA, Al Akel M, Akl EA. The effects of
waterpipe tobacco smoking on health outcomes: an updated sys-
tematic review and meta-­analysis. Int J Epidemiol. 2017;46:32‐43.
11. Chrcanovic BR, Albrektsson T, Wennerberg A. Smoking and
dental implants: a systematic review and meta-­analysis. J Dent.
2015;43:487‐498.
12. Bezerra Ferreira JD, Rodrigues JA, Piattelli A, Iezzi G, Gehrke SA,
Shibli JA. The effect of cigarette smoking on early osseointegration
of dental implants: a prospective controlled study. Clin Oral Implants
Res. 2016;27:1123‐1128.
13. ALHarthi SS, BinShabaib MS, Ahmed HB, Mehmood A, Khan J,
Javed F. Comparison of peri-­implant clinical and radiographic in-
flammatory parameters among cigarette and waterpipe (narghile)
smokers and never-­smokers. J Periodontol. 2018;89:213‐218.
14. Al-Sowygh ZH, Al-Kheraif AA, Akram Z, Vohra F, Javed F. Peri-­
implant soft tissue inflammatory parameters and crestal bone
loss among waterpipe (Narghile) smokers and never-­s mokers
with and without type 2 diabetes mellitus. J Periodontol.
2018;89:645‐652.
15. Booth A, Clarke M, Dooley G, et al. The nuts and bolts of PROSPERO:
an international prospective register of systematic reviews. Sys Rev.
2012;1:2.
16. Moher D, Liberati A, Tetzlaff J, Altman DG; Prisma Group. Preferred
reporting items for systematic reviews and meta-­analyses: the
PRISMA statement. PLoS Med. 2009;6:e1000097.
17. Stang A. Critical evaluation of the Newcastle-­Ottawa scale for
the assessment of the quality of nonrandomized studies in meta-­
analyses. Eur J Epidemiol. 2010;25:603‐605.
18. Borenstein M, Hedges LV, Higgins J, Rothstein HR. A basic introduc-
tion to fixed-­effect and random-­effects models for meta-­analysis.
Res Syn Methods. 2010;1:97‐111.
19. Al-Sowygh ZH, Aldamkh MK, Binmahfooz AM, et al. Assessment of
matrix metalloproteinase-­8 and-­9 levels in the peri-­implant sulcular
fluid among waterpipe (narghile) smokers and never-­smokers with
peri-­implantitis. Inhal Toxicol. 2018;30:72‐77.
20. Abduljabbar T, Akram Z, Vohra F, Warnakulasuriya S, Javed F.
Assessment of interleukin-­1β, interleukin-­ 6, and tumor necrosis
factor-­Α levels in the peri-­implant sulcular fluid among waterpipe
(narghile) smokers and never-­smokers with peri-­implantitis. Clin
Implant Dent Relat Res. 2018;20:144‐150.
AKRAM et al.
21. Shihadeh A. Investigation of mainstream smoke aerosol of the ar-
gileh water pipe. Food Chem Toxicol. 2003;41:143‐152.
22. Monzer B, Sepetdjian E, Saliba N, Shihadeh A. Charcoal emissions
as a source of co and carcinogenic pah in mainstream narghile wa-
terpipe smoke. Food Chem Toxicol. 2008;46:2991‐2995.
23. Aboaziza E, Eissenberg T. Waterpipe tobacco smoking: what is
the evidence that it supports nicotine/tobacco dependence? Tob
Control. 2015;24:i44‐i53.
24. Wu LZ, Duan DM, Liu YF, Ge X, Zhou ZF, Wang XJ. Nicotine fa-
vors osteoclastogenesis in human periodontal ligament cells co-­
cultured with cd4(+) t cells by upregulating il-­1beta. Int J Mol Med.
2013;31:938‐942.
25. AlQahtani MA, Alayad AS, Alshihri A, Correa FO, 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.
26. Ghanem A, Abduljabbar T, Akram Z, Vohra F, Kellesarian SV, Javed
F. A systematic review and meta-­analysis of pre-­clinical studies
assessing the effect of nicotine on osseointegration. Int J Oral
Maxillofac Surg. 2017;46:496‐502.
27. Barao VA, Ricomini-Filho AP, Faverani LP, et al. The role of nicotine,
cotinine and caffeine on the electrochemical behavior and bacterial
colonization to cp-­ti. Mater Sci Eng C Mater Biol Appl. 2015;56:114‐124.
28. Farina R, Filippi M, Brazzioli J, Tomasi C, Trombelli L. Bleeding on
probing around dental implants: a retrospective study of associated
factors. J Clin Periodontol. 2017;44:115‐122.
29. Lindhe J, Meyle J; Group D of the European Workshop on
Periodontology. Peri-­implant diseases: consensus report of the
|
      7 of 7
sixth European workshop on periodontology. J Clin Periodontol.
2008;35:282‐285.
3 0. Javed F, Al-Askar M, Samaranayake LP, Al-Hezaimi K. Periodontal
disease in habitual cigarette smokers and nonsmokers with and
without prediabetes. Am J Med Sci. 2013;345:94‐98.
31. Baab DA, Öberg PÅ. The effect of cigarette smoking on gingival
blood flow in humans. J Clin Periodontol. 1987;14:418‐424.
32. Sakallioğlu EE, Sakallioğlu U, Lütfioğlu M, Pamuk F, Kantarci A.
Vascular endothelial cadherin and vascular endothelial growth fac-
tor in periodontitis and smoking. Oral Dis. 2015;21:263‐269.
33. Tonetti M, Palmer R; Working Group 2 of the VIII European
Workshop on Periodontology. Clinical research in implant den-
tistry: study design, reporting and outcome measurements: con-
sensus report of Working Group 2 of the VIII European Workshop
on Periodontology. J Clin Periodontol. 2012;39:73‐80.
3 4. Moher D, Fortin P, Jadad AR, et  al. Completeness of report-
ing of trials published in languages other than English: implica-
tions for conduct and reporting of systematic reviews. Lancet.
1996;347:363‐366.
How to cite this article: Akram Z, Javed F, Vohra F. Effect of
waterpipe smoking on peri-­implant health: A systematic review
and meta-­analysis. J Invest Clin Dent. 2019;10:e12403. https://
doi.org/10.1111/jicd.12403