DOI: 10.1111/prd.
12282
REVIEW ARTICLE
Tobacco-­product usage as a risk factor for dental implants
Fawad Javed1 | Irfan Rahman2 | Georgios E. Romanos1,3
1
Eastman Institute of Oral Health, University of Rochester, Rochester, NY, USA
2
Department of Environmental Medicine, University of Rochester Medical Center, Rochester, New York, USA
3
Department of Oral Surgery and Implant Dentistry, Dental School, Johann Wolfgang Goethe University, Frankfurt, Germany
Correspondence
Georgios E. Romanos, Department of Periodontology, School of Dental Medicine, Stony Brook University, Stony Brook, New York, USA.
Email: Georgios.Romanos@stonybrookmedicine.edu
KEYWORDS
alveolar bone loss, dental implant, inflammation, osseointegration, smoking
1 | TO BACCO U S E: A R I S K FAC TO R FO R
PE R I - ­I M PL A NT D I S E A S E S
Although dental implants have demonstrated success and survival
rates of up to 100%,1-3 the occurrence of complications, such as
peri-­i mplant diseases (peri-­i mplant mucositis and peri-­i mplantitis),
cannot be disregarded.4 Besides poor plaque control, a history
of periodontal disease, an immunocompromised state (such as
found among patients with AIDS and poorly controlled diabetes
mellitus), and occlusal overloading, a significant risk factor for
peri-­implant diseases is habitual use of tobacco products. 5,6 It
has been reported that tobacco smoke contains over 4000 po-
tential toxins, of which nicotine is considered as one of the most
hazardous and addictive.7 In a recent retrospective clinical study,
Chrcanovic et al 8 investigated the local risk factors associated
with dental implant failure among 2670 participants who had
received 10 096 implants. The results were based on univariate
and multivariate logistic regression models and showed that to-
bacco smoking is a statistically significant predictor of dental im-
plant failure. 8 Similarly, the results from a systematic review and
9
meta-­a nalysis also showed that the rates of implant failure, post-
operative infections, and peri-­implant crestal bone loss are statis-
tically significantly higher in smokers compared with nonsmokers.
Furthermore, it has also been reported that Type IV bone (which
exhibits poor cortical thickness, low trabecular density, and poor
medullary strength) is seen more often among smokers than
among nonsmokers.10 Although dental implants can remain func-
tionally stable in smokers and among patients with poor bone
11-13
quality, it is imperative to recognize the detrimental effects
of nicotine (a major tobacco constituent) on peri-­implant tissues
which may lead to implant failure.
48  |  wileyonlinelibrary.com/journal/prd
© 2019 John Wiley & Sons A/S.
Published by John Wiley & Sons Ltd
2 | N I COTI N E: D E FI N ITI O N A N D IT S
D E LE TE R I O U S E FFEC T S O N O R A L A N D
S YS TE M I C H E A LTH
Nicotine is found in the leaves of the tobacco plant, Nicotiana ta-
bacum. Nicotine is a para-­
sympathomimetic alkaloid and a psy-
chostimulant drug, which has a half-­life of 2 hours, in contrast to
cotinine (a principal metabolite of nicotine) which has a half-­life of
15-­20  hours.14 Nearly 90% of nicotine is metabolized by the liver,
lungs, and kidneys. The dopaminergic properties of nicotine make it
highly addictive.15
The oral cavities of tobacco smokers and users of smokeless
tobacco products are exposed to high concentrations of nicotine.
It has been reported that, among smokers, the concentration of
nicotine can be up to nearly 300 times higher in gingival crevicular
fluid than in serum.16 Studies17-19 have hypothesized that the vaso-
constrictive effects of nicotine result in reduced bleeding on prob-
ing (a classical marker of periodontal disease) in smokers compared
with nonsmokers. High concentrations of nicotine and cotinine have
adverse effects on the proliferation of human gingival fibroblasts
and their adhesion to root surfaces, thereby compromising gingi-
val clinical attachment levels. 20 Nicotine enhances the growth and
proliferation of osteoclasts that increase alveolar bone loss. 21,22
Furthermore, nicotine has also been associated with increased ex-
pression of advanced glycation end products and their receptors in
the periodontal tissues of smokers, which may compromise the out-
come of periodontal surgical interventions in these individuals. 23,24
Systemically, chronic exposure to nicotine has been associated
with acute cardiac ischemic events, atherosclerosis, coronary ar-
tery disease, hypertension, and thrombosis. 25,26 Nicotine expo-
sure has also been reported to increase the malignant potential of
Periodontology 2000. 2019;81:48–56.
JAVED et al. |
      49

pancreatic cancer stem cells and trigger the apoptosis of cardio-
27,28
myocytes. Furthermore, nicotine impairs the function of poly-
morphonuclear leukocytes and causes hypercoagulation of blood
as a result of increased platelet activation and raised fibrinogen
levels29,30 (Figure 1).
3 | E FFEC T O F N I COTI N E O N
OS S EO I NTEG R ATI O N : LE S S O N S FRO M
ANIMAL STUDIES
To our knowledge from the indexed literature, the effect of
nicotine on osseointegration has been assessed in only a lim-
31-38
ited number of animal studies. Amongst these, 4 studies
were performed in rabbits 31,32,35,37 and 4 in rodents. 33,34,36,38
In these studies, 31-38 the outcome variables used for the as-
sessment of osseointegration included bone area, bone volume,
bone-­t o-­i mplant contact, bone density, removal torque test, and
33
resonance frequency analysis. In the studies by Berley et al
and Yamano et al 38 there was a statistically significant decrease
in bone-­to-­implant contact among rats exposed to nicotine at
4 weeks of follow-­u p compared with unexposed rats. Soares
et al 36 showed that bone volume around implants was markedly
lower in rats that received subcutaneous injections of nicotine
than in control rats. However, some studies 31,32,34,35,37 report
no statistically significant difference in bone-­to-­implant con-
tact between animals with or without exposure to nicotine.
However, it is important to interpret these results with caution
as nicotine was administered to the animals subcutaneously in
these studies. 31,32,34,35,37 It has been reported that drug (nico-
tine) absorption is faster when inhaled than when administered
subcutaneously. 39 Therefore, it is likely that the subcutaneous
injections of nicotine used in these studies 31,32,34,35,37 were
unable to demonstrate its true effects on osseointegration
because of the slow absorption of nicotine into the systemic
circulation.
4 | S U CC E S S A N D S U RV I VA L O F
I M PL A NT S A N D TO BACCO PRO D U C T
U S AG E
4.1 | Cigarette smoking
A classical risk factor for peri-­implant diseases and implant failure
is cigarette smoking.4,10,40 Levin et al41 reported that peri-­implant
marginal bone loss is statistically significantly higher in cigarette
smokers than in ex-­smokers and nonsmokers. One explanation in
this regard is that nicotine increases the production of inflamma-
tory cytokines (such as interleukin-­6 and tumor necrosis factor-­
alpha) by osteoblasts.42 However, controversial results have also
previously been reported. In a study by Romanos et al,11 platform-­
switched implants were placed in smokers (individuals who had
smoked at least 20 cigarettes daily for over 10 years) and non-
smokers using the same treatment protocol. All implants were im-
mediately loaded and the mean follow-­up periods in smokers and
nonsmokers were approximately 5 and 9 years, respectively. At fol-
low-­up, implant survival rates were 97% among smokers and 99%
among nonsmokers.11 The study concluded that long-­term clinical
outcomes for immediately loaded platform-­shifted implants placed
in smokers and nonsmokers are comparable provided that the
abutments are placed on the day of surgery and never removed.11
4.2 | Waterpipe smoking
Waterpipe (synonyms: hookah, hubble bubble, narghile, and shee-
sha) is a type of tobacco smoking in which charcoal-­h eated air

Tobacco
products/Nicotine

Effects on periodontal health Effects on a molecular level Effects on systemic health

1. Acute cardiac ischemia

1. Impairs function of
1. Vasoconstriction of gingival 2. Atherosclerosis
polymorphonuclear leukocytes
blood vessels. 3. Bronchitis
2. Impairs structure and function
2. Pale gingival tissues 4. Cardiomyocytes apoptosis
of gingival fibroblasts.
3. Increased periodontal 5. Coronary artery disease
3. Increases platelet
pocketing 6. Hepatic cancer
adhesiveness.
4. Increased clinical 7. Hypertension
4. Suppresses the growth of
attachment loss and 8. Pancreatic cancer
osteoblast-like cells
marginal bone loss 9. Stroke
5. Increases oxidative stress,
F I G U R E   1   A diagrammatic 5. Impaired adhesion of 10. Thrombosis
inflammation and
representation of the deleterious effects fibroblasts to root surfaces 11. Throat irritation
myofibroblast differentiation
of nicotine in health
 |
50       JAVED et al.

passes through perforated aluminium foil and across powdered
tobacco to become smoke, which is bubbled through water be-
fore being inhaled (Figure 2). Waterpipe smoking is a cultural norm
in many countries, such as Bahrain, Egypt, Israel, Kuwait, Qatar,
Saudi Arabia, and the United Arab Emirates.43-51 However, water-
pipe smoking has gained popularity in many developed countries,
such as Australia, Canada, the UK, and the USA, particularly among
young individuals. 52-57 Waterpipe smokers often consider water-
pipe smoking as less harmful than traditional cigarette smoking as
the tobacco smoke in waterpipes is filtered through water, which
absorbs nicotine. Moreover, many individuals start waterpipe
smoking in an attempt to quit cigarette smoking. 58 The prevalence
of systemic conditions, such as hypertension, tachycardia, and oxi-
dative stress, has been reported to be higher in waterpipe smokers

Tobacco bowl covered with

perforated aluminium foil that
houses charcoal

Ash-tray

Body

One way valve for smoke release Hose connector

Mouth piece
Rubber air sealer

Hose

Water tank/bowl

F I G U R E   2   Illustration of a waterpipe
and its components

TA B L E   1   Studies assessing the effect of waterpipe smoking on periodontal and peri-­implant inflammatory parameters

Periodontal status in waterpipe smokers Peri-­implant status in waterpipe smokers

Study/ Outcome of study compared with Study/ Outcome

Reference Study design nonsmokers Reference Study design of study

Baljoon Cross-­sectional The prevalence and severity of

et al.44 Retrospective vertical periodontal bone defects
was nearly 3 times higher in
waterpipe smokers
No studies in
Bibars et al.67 Cross-­sectional Increased plaque index, clinical
Retrospective attachment loss, and probing indexed literature
depth ≥4 mm in waterpipe
smokers
Javed et al.46 Cross-­sectional Increased plaque index, probing
Retrospective depth ≥4 mm, clinical attachment
loss, marginal bone loss, and
reduced gingival bleeding in
waterpipe smokers
Natto et al.63 Cross-­sectional Increased plaque index and reduced
Retrospective gingival bleeding in water pipe
smokers
Natto et al. 50 Cross-­sectional The relative risk of periodon-
Retrospective tal bone loss was 3.5-­fold higher in
waterpipe smokers
JAVED et al.
TA B L E   2   Studies assessing the effect of cigar and pipe smoking on periodontal and peri-­implant inflammatory parameters
Periodontal status in cigar and pipe smokers
Outcome of study compared with
Study/Reference Study design nonsmokers
Albandar et al.76 Cross-­sectional Higher prevalence of moderate
Retrospective and severe periodontitis in cigar
and pipe smokers
Feldman et al.74 Cross-­sectional No difference
Retrospective
Krall et al.77 Cross-­sectional Increased probing depth, gingival
Retrospective bleeding, tooth mobility, and
marginal bone loss in cigar and
pipe smokers
than in nonsmokers. 59,60 Waterpipe smoking has also been associ-
ated with the development of lung cancer. 61 Studies 46,62-64 have
shown that, similarly to cigarette smoking, waterpipe smoking is a
risk factor for oral cancer, periodontal disease, and alveolar bone
loss. One explanation for this is that during waterpipe smoking and
cigarette smoking, individuals are exposed to the same chemicals,
namely nicotine, tar, oxidants, polyaromatic hydrocarbons, and
65,66
carbon monoxide. There is a possibility that the nicotine and
chemicals associated with waterpipe smoking induce a state of
oxidative stress in peri-­implant tissues (gingiva and alveolar bone),
thereby increasing the likelihood of peri-­implant disease devel-
opment via inflammatory responses, which if left uncontrolled
will lead to implant failure/loss. It is therefore hypothesized that
waterpipe smoking is a significant risk factor for peri-­implant dis-
eases; and peri-­implant bleeding on probing, probing depth, and
marginal bone loss are higher among cigar/pipe smokers than in
nonsmokers. However, to date, there are no studies in indexed lit-
erature that have assessed this hypothesis. It has also been stated
that global attention against waterpipe smoking is needed and that
it should not be considered as an alternative and safe way of smok-
67
ing. There is a need for long-­term prospective and retrospective
clinical studies that assess the influence of waterpipe smoking on
peri-­implant inflammatory parameters (Table 1).
4.3 | Pipe and cigar smoking
Pipe and cigar smoking are common in many parts of the world,
including the USA, and the habit is particularly common among
68-70
individuals of privileged socioeconomic groups. The toxic con-
stituents in cigar and pipe smoke are similar to those in cigarette
71,72
smoke ; however, cigar smoke has been shown to have higher
levels of tobacco-­specific nitrosamines than cigarette smoke as a
result of the curing and fermentation process used to produce cigar
tobacco.71,72 Wald and Watt73 suggested that cigarette smokers who
have difficulty in quitting smoking may smoke cigars or pipes as the
quality of tobacco smoked and inhaled during cigar or pipe smok-
74
ing is lower than that of cigarettes. In the study by Feldman et al,
calculus deposition, probing depth, and alveolar bone loss were
|
      51
Peri-­implant status in cigar and pipe smokers
Study/ Outcome
Reference Study design of study
No studies in
indexed literature
significantly higher in cigarette smokers than in pipe/cigar smokers.
However, cigar and pipe smoking is as hazardous to health as ciga-
rette smoking.71,75 Studies76,77 have shown that the prevalence of
moderate and severe periodontitis is significantly higher in cigar and
pipe smokers than in nonsmokers. Albandar et al76 predicted that
the prevalence of moderate and severe periodontitis among cigar/
pipe smokers is 17.6%. This study76 also showed that the number
of sites with clinical attachment loss of ≥5 mm, probing depth of
≥3 mm, and gingival recession were significantly higher in cigar/pipe
smokers than in nonsmokers (Table 2).
4.4 | Electronic cigarette vaping
An electronic cigarette is a battery-­operated device that consists of:
(a) a metal heating element in a stainless-­steel casing; (b) a container;
(c) an atomizer; and (d) a battery. The container is filled with liquid,
which usually contains nicotine, propylene glycol, glycerin, and arti-
ficial flavorings. A variety of aldehydes, such as acrolein, acetalde-
hyde, and formaldehyde, are present in the aerosols from electronic
cigarettes.78,79 The heating device converts the liquid into vapor that
is inhaled in the same manner as during traditional tobacco smoking.
Individuals attempting to quit smoking believe that vaping electronic
cigarettes is an effective way to intake nicotine. Although studies
demonstrating the detrimental effects of electronic cigarette smok-
ing on health are scare, experimental studies have shown that ex-
posure to electronic cigarette aerosols increases inflammatory and
genotoxic stresses and induces DNA fragmentation in lung fibro-
blasts.80,81 In addition, increased production of destructive inflam-
matory cytokines (interleukins 6 and 8) in lung fibroblasts has also
been associated with vaping.80,81 Interestingly, results from a recent
in vitro study82 showed that electronic cigarettes with flavorings
enhance oxidative stress and increase the release of destructive in-
flammatory cytokines (interleukin-­8 and prostaglandin E2) in human
periodontal ligament fibroblasts, pooled human gingival epithelial
progenitor cells, and epigingival three dimensional epithelium. In a
pilot study, Wadia et al83 compared the gingival status of smokers be-
fore and after substituting smoking tobacco with vaping. The results
showed a significant increase in gingival inflammation when tobacco
 |
52       JAVED et al.
A B C D
Brand name
Manufacturers’ name
F I G U R E   4   Various commercially available smokeless tobacco products. (A) gutka; (B) betel-­quid; (C) shamma; (D) naswar; and (E) snuff
smokers switched to vaping from smoking83; however, these results
should be interpreted with caution as they are based on a pilot study.
Results from a recent review article suggest that vaping plays a role
in the etiology of periodontal diseases and oral premalignant lesions,
84
such as oral submucous fibrosis. A proposed immunoinflammatory
mechanism associated with peri-­implant inflammation and bone loss
in vaping individuals is shown in Figure 3. To our knowledge, there
are no clinical studies assessing the effect of electronic cigarette
smoking on periodontal and peri-­implant bone and soft tissues. From
the level of experimental evidence currently available, it seems that
electronic cigarette smoking may negatively influence the outcome
of dental implant therapy in a manner similar to conventional smok-
ing by enhancing oxidative stress in periodontal and peri-­implant
tissues and augmenting alveolar bone loss. Hence, well-­designed
clinical studies are needed in this regard.
5 |  S U CC E S S A N D S U RV I VA L O F
I M PL A NT S A N D S M O K E LE S S TO BACCO
U S AG E
The use of smokeless tobacco products is common globally.
Smokeless tobacco products are consumed orally or nasally without
burning tobacco. Smokeless tobacco products are commonly placed
F I G U R E   3   A proposed immuno-­
inflammatory mechanism associated with
peri-­implant inflammation and bone loss
in vaping individuals. AGEs, advanced
glycation end products; IL, interleukin;
PGE2, prostaglandin E2
E
in the buccal vestibule and lower labial sulcus and sucked intermit-
tently. The contents may either be swallowed or spat out when de-
sired. Various forms of smokeless tobacco products commercially
available in global markets are shown in Figure 4. Although the
products shown in Figure 4A-­D are commonly consumed in many
South Asian and Middle Eastern countries (including India, Pakistan,
Bangladesh, Nepal, Sri Lanka, Yemen, and Saudi Arabia), their un-
controlled export to developed countries has made them available
to communities in many countries, including the USA, the UK, and
Australia. However, snuff is the most common form of smokeless
tobacco product used in many European countries and the USA.85,86
There is abundant evidence showing a direct association between
consumption of smokeless tobacco products and the occurrence of
oral premalignant and malignant lesions.87,88 A number of studies89-96
have assessed periodontal health status among users of smokeless
tobacco products and controls (eg, individuals not using tobacco in
any form). Studies89,95 that compared the periodontal inflammatory
effects of different types of smokeless tobacco product have shown
that all types of smokeless tobacco are equally hazardous to peri-
odontal health and none of the smokeless tobacco products can be
considered as less hazardous than any other (Table 3).
Upon a careful review of indexed literature, there was only 1
study 97 that assessed the rates of infection in tobacco users (in-
cluding smokeless tobacco) having undergone hip arthroplasty. The
JAVED et al. |
      53

TA B L E   3   Studies assessing the effect of smokeless tobacco product use on periodontal and peri-­implant inflammatory parameters

Periodontal status in smokeless tobacco product users Peri-­implant status in smokeless tobacco product users

Study/ Type of smokeless Outcome of study compared Study/ Type of smokeless Outcome
Reference tobacco assessed with controls Reference tobacco assessed of study

Al-­A skar Gutka and Shamma Increased PI and BOP, and

et al.89 PD ≥ 4 mm in smokeless
tobacco users
Javed et al.91 Gutka Increased PI and BOP, and No studies in
PD ≥ 4 mm in smokeless
tobacco users indexed literature
95
Javed et al. Betel-­quid Increased PI and BOP, and
PD ≥ 4 mm in smokeless
tobacco users
Robertson Snuff Increased gingival recession and
et al.96 clinical attachment loss in
smokeless tobacco users

BOP, bleeding on probing; PD, probing depth; PI, plaque index.

results showed that tobacco use was associated with a high risk of
deep infection around hip implants. It is important to interpret these
results with caution as patients using different types of tobacco
product, including smokeless tobacco, cigarettes, pipes, and cigars,
were included.97 However, there are no studies in the indexed lit-
erature that have assessed the use of smokeless tobacco products
in relation to their effect on dental implants. Nicotine is an integral
component of the tobacco contained in smokeless tobacco products
and jeopardizes periodontal health; accordingly, it is hypothesized
that (a) peri-­implant inflammatory parameters (peri-­implant bleed-
ing on probing, probing depth, and marginal bone loss) are worse in
smokeless tobacco product users than in controls and that (b) peri-­
implant inflammatory parameters are worse around implants located
in the buccal vestibule in which smokeless tobacco product is placed
compared with implants on the contralateral side. Additional studies
are needed to test these hypotheses.
interactions between advanced glycation end products and their
receptors remain uninvestigated. It has recently been shown that
electronic cigarette vaping induces oxidative stress and damaging
responses via enhancing the interactions between advanced gly-
cation end products and their receptors and through stimulating
prostaglandin E2 release by periodontal ligament fibroblasts and
epithelium. 82 Therefore, it is perceived that other nicotinic prod-
ucts can have repercussions on implant rejection and peri-­i mplant
diseases.
It is imperative for health-­care providers to be aware of the det-
rimental effects of tobacco products on oral health. It is also rec-
ommended that health-­care providers educate patients (particularly
those undergoing periodontal and implant therapies) about the del-
eterious effect of tobacco products on oral health.
7 | CO N C LU S I O N

6 | TO BACCO PRO D U C T S A N D
DA M PE N I N G O F I N N ATE I M M U N E
R E S P O N S E S I N S U RV I VA L /FA I LU R E O F
D E NTA L I M PL A NT S
It is known that conventional tobacco smoking can lead to damp-
ening of innate immune responses via activation of the nuclear
factor kappa B pathway and toll-­like receptors.98,99 It is hypoth-
esized that dampening of the immune response triggers vari-
ous inflammatory mediators and oxidative stress, culminating in
further damage to peri-­implant tissues, which may lead to peri-­
implant diseases and ultimately to implant loss if left untreated.
Although conventional smoking is known to enhance the inter-
actions between advanced glycation end products and their re-
ceptors and to induce oxidative stress in periodontal tissues, the
association of other habits (waterpipe, cigar, pipe, and smokeless
tobacco product usage) with induction of oxidative stress and the
Even though scientific data on the effect of tobacco products on
the success and survival of dental implants are scarce, the deleteri-
ous effects of nicotine-­containing products on peri-­implant tissues
cannot be disregarded. Therefore, to minimize the negative effects
of tobacco on periodontal and peri-­implant tissues and thus improve
public health, special smoking-­cessation programs should be devel-
oped and patients educated appropriately.
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How to cite this article: Javed F, Rahman I, Romanos GE.
Tobacco-­product usage as a risk factor for dental implants.
Periodontol 2000. 2019;81:48–56.
https://doi.org/10.1111/prd.12282