International Dental Journal 2016; 66: 29–35

SCIENTIFIC RESEARCH REPORT

doi: 10.1111/idj.12192

Comparison of clinical periodontal status among habitual

smokeless-tobacco users and cigarette smokers
Varun Kulkarni1, Juhi Raju Uttamani1 and Neel B Bhatavadekar2,3
1
Department of Periodontics, University of Illinois at Chicago, Chicago, IL, USA; 2Clarus Dental Specialities, Pune, India; 3University of
Texas Health Science Center, Houston, TX, USA.

Aim: Investigating the comparative effect of cigarette smoking and smokeless-tobacco use on periodontal health. Back-
ground: There is a dearth of studies comparing the effects of smoking and smokeless tobacco on periodontal health.
Smokeless tobacco is emerging as a major public health hazard, but is often neglected as a risk factor by many clinicians.
Materials and methods: A cross-sectional study of 286 subjects was conducted. The participants were divided into mutu-
ally exclusive groups (i.e. any subject who had the habit of both smoking as well as smokeless tobacco usage was
excluded from the study), as follows: a smoking group (SG; n = 121); a smokeless-tobacco group (ST; n = 81); and a
non-tobacco-consuming group (NT; n = 84). Data were obtained using a questionnaire and by clinical examination. The
Periodontal Disease Index (PDI) and Oral Hygiene Index-Simplified (OHI-S) were used to clinically evaluate the period-
ontal and dental health status of the subjects. Multivariate analysis was performed to identify statistical correlations.
Results: The Plaque Index was higher in the ST group than in the SG group and was statistically significantly higher in
the ST group than in the NT group. Probing depth and gingival inflammation (components of the PDI) were also higher
in the ST group than in the SG and NT groups, but this was not statistically significant. Conclusions: Within the limits
of the study, and for this study population, the impact on the periodontium as a result of smokeless tobacco use
appeared to be comparable with that of smoking tobacco. The results of this study affirm the need to consider smokeless
tobacco as a possible contributory factor to periodontal disease, in addition to smoking, and to counsel patients
accordingly. Further randomised clinical trials are necessary to validate the long-term impact of smokeless tobacco on
periodontal disease.

Key words: Smokeless tobacco, smoking, periodontal disease, oral hygiene status, rural

been widely neglected in clinical treatment proto-

INTRODUCTION
cols10.
Periodontitis not only causes tooth loss but has also A recent Cochrane database review article has
been shown to be a risk factor for systemic diseases, assessed the adverse effects of prolonged use of smo-
such as diabetes1,2. According to a report from the keless tobacco11. This study found an association
European Society of Cardiology, there is a moderate between smokeless tobacco and oral cancer and
association between periodontal disease and coronary cardiovascular disease11. The 2011 National Youth
heart disease1–3. Tobacco Survey, which gauged the nationwide (USA)
Scientific evidence has noted the harmful effects of use of conventional (chewing tobacco, snuff) and novel
smoking on the periodontium2. Many epidemiological (snus, other dissolvable tobacco products) smokeless
studies have demonstrated that smoking is a strong tobacco products, concluded that the prevalence of
contributing factor to periodontal disease4–7. The smokeless tobacco use was 5.6%12. The authors also
association of smokeless tobacco with various concluded that smokeless tobacco usage was associated
periodontal parameters, such as bleeding on probing with less harmful effects than cigarette smoking, which
and probing depth, has been explored in a limited could be a factor leading to wider use.
number of previous studies8,9. Although smoking is Smokeless tobacco has been linked previously with
acknowledged as a major contributory factor in peri- tooth loss13. Tooth loss was found to be statistically
odontal disease, the impact of smokeless tobacco has higher in smokeless tobacco users (56%) and in
© 2015 FDI World Dental Federation 29
Kulkarni et al.

patients smoking tobacco (58%) compared with non- Hospital, Virar, Mumbai, from June 2012 to Decem-
users of tobacco (28%)14. It has also been established ber 2012. The study was conducted after obtaining
that smokeless tobacco users have a higher prevalence Institutional Review Board (IRB) approval from the
of recession14, and when data are stratified according in-house ethical board of the Ramkrishna Mission’s
to years of use, subjects using smokeless tobacco Charitable Trust, in full accordance with the World
for 10-18 years exhibit the greatest difference as Medical Association Declaration of Helsinki.
compared with non-users.
A report15 analysing data from the 2011 Youth
Sample size calculation and inclusion/exclusion
Risk Behavior Surveillance System survey assessed the
criteria
use of smokeless tobacco and smoking in the adoles-
cent US population and reported that male subjects The population size of the study was calculated a
rather than female subjects were more likely to use priori. It was determined that 267 subjects were nec-
smokeless tobacco. One conclusion derived from the essary to detect a minimum effect size for the survey
study was that the use of smokeless tobacco needs to with an alpha error of 5%, 80% power and a confi-
be accounted for when drafting tobacco-cessation pro- dence level of 95%. Patients with any terminal medi-
grammes. cal illness, hypertension and/or diabetes, and
The literature on smokeless tobacco and periodon- pregnant and lactating women, were excluded. Only
tal disease is not without controversy16,17. Although those patients smoking more than five cigarettes per
the vast majority of reports demonstrate a positive day for the past 2 years or more were included in
relationship between smokeless tobacco use and peri- the smoking group (SG). The smokeless tobacco (ST)
odontal disease, there are reports which appear to group comprised subjects who had consumed smoke-
show that the use of smokeless tobacco (and, in par- less tobacco on a daily basis for the past 2 years or
ticular, Swedish snus) is not related to a higher risk more. Two types of smokeless tobacco used by the
for periodontitis18. study population were gutka and creamy snuff. After
Some earlier surveys showed that tobacco placed in providing written informed consent, all participants
the mouth, cheek or lip vestibule resulted in an were asked to fill in the study questionnaire. Each
increased incidence of periodontitis8,14. In general, the patient’s oral health behaviour was noted on the
prevalence of these habits is lowest in population basis of their brushing habits. Also, basic information
groups with the highest educational level11. Oral (age, gender, socio-economic status, education level
health is also typically more neglected in rural areas and occupation) and medical and dental history were
compared with urban areas8,10,19. In developing coun- noted. A periodontal clinical examination was con-
tries, for instance, 80% of dentists practice in urban ducted to assess parameters such as bleeding on
metropolitan cities, whereas 70% of the population probing (BOP), probing depths (PD) and plaque/de-
resides in villages10,19. This finding has tremendous bris index, as detailed below.
significance from the point of establishing a tobacco-
cessation health-outreach policy in these countries.
Clinical oral examination
Thus, although smokeless tobacco is a major health
hazard, not many large cross-sectional studies have The Periodontal Disease Index (PDI)22 and the Oral
been published, and those which have been published Hygiene Index-Simplified (OHI-S)23 were used to
have a relatively small sample size8,14. Notably, the determine the periodontal status and the dental health
authors of this publication could not find a published status, respectively, of the subjects. Six index teeth
study comparing periodontal parameters across three (Ramjford teeth) of each individual were assessed for
groups: smokers; smokeless tobacco users; and non- the presence of debris, plaque, calculus, BOP, gingival
tobacco control. Tobacco use increases the risk of inflammation, clinical attachment loss (CAL) and
diabetes and heart disease, both of which are linked to pocket formation on all five tooth surfaces (occlusal,
an increased risk of periodontal disease20–22. buccal/labial, lingual/palatal, mesial and distal). In
The aim of the current study was therefore to fill the order to minimise interexaminer differences, PD was
existing void in the published literature. Compared measured using a Williams probe by the authors J.U.
with previous reports of this nature1,8–10,19 (where the and V.K, individually on the same patient, rounding
studies are mainly questionnaire-related surveys), this up to the nearest millimetre, with the mean value con-
study has a clinical assessment component. sidered as the final reading.
The PDI was determined and scored 23–25 as: score 0,
absence of inflammation (normal gingiva); score 1, mild
MATERIALS AND METHODS
inflammation (slight change in colour, slight oedema,
This cross-sectional study was conducted in the dental no BOP); score 2, moderate inflammation (moderate
unit of Ramkrishna Mission’s Charitable Trust’s glazing, redness, oedema and BOP); score 3, severe
30 © 2015 FDI World Dental Federation
 Effect of smokeless tobacco on periodontal health

inflammation (marked redness and hypertrophy, ulcer- them, 121 were using smokeless tobacco; 81 were
ation and tendency for spontaneous bleeding)24. The smokers; and 84 subjects neither smoked nor con-
periodontal pocket depth and CAL for chronic peri- sumed tobacco. All groups were mutually exclusive
odontitis was categorised into mild, moderate and sev- (i.e. to avoid misinterpretation of the results, we
ere periodontitis, as follows. Mild periodontitis25 excluded from the study any subject who had the habit
(score 4)23: gingival inflammation and bleeding on of both smoking as well as using smokeless tobacco.
probing, periodontal pocket depth ≤4 mm and CAL of Along with basic data about the participants and
1–2 mm. Moderate periodontitis25 (score 5)23: gingival the medical and dental history, information was
inflammation, BOP, presence of suppuration, periodon- obtained regarding the toothbrushing frequency per
tal pocket depth ≤6 mm, CAL of 3–4 mm and possible day, usage of fluoridated dentifrice and usage of mou-
presence of slightly loose teeth. Severe periodontitis25 thrinse, as well as dental visits in the past 2 years and
(Score 6)23: obvious inflammation or occurrence of average income (Table 1). It was seen that 54% of
periodontal abscess, periodontal pocket depth >6 mm, respondents indicated brushing once a day, 28%
CAL of ≥5 mm and more than one loose tooth. brushed twice a day, 16% of the population did not
The plaque component of the PDI was calculated brush at all and only 2% of the subjects brushed more
using the Plaque Index26 (PI), obtained using a mouth than twice a day; mouthwash was used by one-sixth
mirror, a dental explorer after air drying of teeth and of all subjects. Oral hygiene habits (toothbrushing and
basic fuschin plaque-disclosing agent. When a desig- mouthrinse use), dental visit within the past 2 years
nated tooth was missing, the closest tooth distal to and income status did not show a statistical correla-
the missing tooth was assessed. Calculus and debris tion with the plaque level. As reported in Table 1,
were calculated using the OHI-S. Calculus was mea- 190 of these 286 subjects had a very low monthly
sured using visual examination or by tactile examina- income.
tion using a mirror and sickle-type dental explorer Table 2 demonstrates the distribution of partici-
(#23) and was scored as follows: 0, absent; 1, mild or pants across each of the attributable scoring criteria
supragingival calculus covering not more than one- for the chosen study parameters (plaque, debris, calcu-
third of the exposed tooth surface; 2, moderate or lus, gingival inflammation, BOP and PD). Figure 1
supragingival calculus covering more than one-third exhibits the statistical association between the peri-
but not more than two-thirds of the tooth surface or odontal parameters and the study groups. The inci-
the presence of individual flecks of subgingival calcu- dence and extent of calculus was significantly higher
lus around the cervical portion of the tooth or both; in the SG group than in the ST group and the NT
3, severe or supragingival calculus covering more than group (P ≤ 0.01). The ST group had the highest per-
two-thirds of the exposed tooth surface or a continu- centage of sites with PD > 6 mm (28%), compared
ous heavy band of subgingival calculus around the with the SG (13%) and the NT (7%) groups. Simi-
cervical portion of the tooth (or both)27. The Debris larly, a higher proportion of patients in the ST (91%)
Index (DI) was calculated in a similar manner. and SG (85%) groups had greater BOP compared
with patients in the NT group (17%) (Table 2), point-
ing to a marked presence of inflammation in both the
Statistical analysis
ST and SG groups. However, the gingival inflamma-
Data analysis was carried out using SPSS version 17 tion scores between groups were not statistically sig-
(IBM SPSS, Chicago, IL, USA). Percentages, propor- nificant, although they showed a tendency to be
tions, mean and standard deviation, and multivariate higher for the ST group.
analysis were calculated, using the chi-square test, PI index was statistically significantly higher in the
between the number of subjects per group and the ST group than in the NT group (P ≤ 0.05) and was
risk factors. The t-test was used to test the relation- higher (although not statistically significantly so) in
ship between plaque score and oral hygiene habits, the ST group than in the SG group. PD also showed a
dental visit and income. P ≤ 0.05 was considered as tendency to be higher in the ST group; however, this
statistically significant. The 95% confidence interval was not statistically significant. Debris Index was not
was calculated, and analysis of variance (ANOVA) statistically significant between groups, but was higher
was used to determine significant difference between in the ST and SG groups compared with the NT
the mean scores of the periodontal risk markers group.
assessed and tobacco consumption/smoking.
DISCUSSION
RESULTS
There is significant evidence relating smoking to peri-
A total of 286 patients (169 men and 117 women; 20– odontal disease5,28,29. However, for the most part, the
50 years of age) participated in the study. Amongst detrimental role of smokeless tobacco has not been
© 2015 FDI World Dental Federation 31
Kulkarni et al.

Table 1 Relationship of oral hygiene habits, dental visit and income with plaque score
Domain Item No. of subjects Plaque score Relationship with
(total n = 286) (mean  SD) plaque score

Oral hygiene Frequency of toothbrushing

habits None 46 1.69  0.61 P = 0.118*
Once a day 155 1.52  0.44
Twice a day 80 1.37  0.65
More than twice a day 5 1.21  0.49
Use of fluoridated toothpaste
Yes 97 1.27  0.34 P = 0.25
No 189 1.35  0.72
Use of mouthwash
Yes 45 1.46  0.15 P = 0.38
No 241 1.39  0.58
Dental visit in Yes 78 1.31  0.66 P = 0.27
last 2 years No 208 1.49  0.13
Income Average 96 1.35  0.75 P = 0.2
(Rs.10,000–25,000/month,
equivalent to $US 385–153/month)
Low 190 1.38  0.63
(Rs. 10,000 or below/month,
equivalent to $US153 or below/month)

*Responses were grouped and paired into four categories (none, once a day, twice a day and more than twice a day). P-values were calculated
using the t-test.
Rs: Indian rupees.

Table 2 Distribution of patients across the three

ment in smokeless tobacco users. Another publica-
study groups
tion30 concluded that habitual gutka (tobacco mixed
Parameter Smokeless Smokers (SG) Non-users of with betel-quid mixture) usage can lead to oral muco-
tobacco (ST) tobacco (NT) sal disorders, and its effects could extend beyond the
(n = 121) (n = 81) (n = 84)
bounds of the oral cavity; these lesions have the ten-
Plaque dency to become malignant31. It has been observed
Score 0 6 (4.95) 6 (7.63) 36 (43.04)
Score 1 32 (26.44) 15 (18.51) 27 (32.33)
that among adolescents in the USA12, the use of
Score 2 50 (41.34) 37 (45.67) 12 (15.47) smokeless tobacco is associated with lower perception
Score 3 33 (27.47) 23 (28.39) 9 (10.96) of harm. In another survey it was reported that ado-
Debris
Score 0 6 (5.20) 5 (6.20) 38 (45.50)
lescents engaged in smokeless tobacco usage were
Score 1 33 (27.70) 14 (17.50) 25 (30.20) more likely to smoke and indulge in other risk-taking
Score 2 51 (42.21) 37.5 (46.30) 17 (20.70) behaviours, such as excessive drinking15.
Score 3 31 (25.30) 66 (30.00) 4 (4.60)
Calculus
The current study is one of the few to assess the
Score 0 7 (5.78) 5 (6.17) 32 (38.09) effects of both smoking and smokeless tobacco con-
Score 1 36 (29.75) 18 (22.22) 31 (36.90) sumption on periodontal parameters. It also is the first
Score 2 48 (39.66) 36 (44.44) 12 (14.28)
Score 3 30 (24.79) 22 (27.16) 9 (10.71)
ever cross-sectional survey conducted on oral health
Gingival inflammation status and sociodemographics in the rural population
No 10 (8.26) 11 (13.58) 47 (55.95) of Mumbai, India. Our report thus seeks to fill the
Mild/moderate 71 (58.67) 51 (62.96) 26 (30.95)
Severe 40 (33.05) 19 (23.45) 11 (13.09)
void in the literature available on tobacco consump-
Bleeding on probing tion in India as well as in Asian, African and North
Present 111 (91.73) 69 (85.18) 15 (17.85) American nations19,32–34.
Absent 10 (8.26) 12 (14.81) 69 (82.14)
Pocket Depth (as per the PDI)
Although tobacco is consumed in numerous ways,
Score 0 8 (6.61) 8 (9.87) 46 (54.76) cigarette smoking is the most prevalent form of use4.
(no pocket) Beedi (a thin cigarette made with tobacco wrapped in a
Score 4 (≤4 mm) 37 (30.57) 22 (27.16) 24 (28.57)
Score 5 (4–6 mm) 42 (34.71) 40 (14.38) 8 (9.52)
Bauhinia racemosa leaf) has been found to be one of
Score 6 (>6 mm) 34 (28.09) 11 (13.58) 6 (7.14) the most popular forms of tobacco smoked in several
countries in South East Asia, as well as in the Middle
Values are given as n (%).
PDI, Periodontal Disease Index. East10. Cigarette smokers have shown a higher inci-
dence of severe periodontitis than snus users18. It has
fully studied. A study conducted14 on the rural male also been shown that smokers have a four-fold
population in Ohio concluded that the occurrence and increased risk of periodontitis compared with non-
extent of gingival recession is linked with site place- smokers35. In our current study, more than half of the
32 © 2015 FDI World Dental Federation
 Effect of smokeless tobacco on periodontal health

ST SG NT Tobacco Product (MRTP) by the company ‘Swedish

7
* * Match’, which also states that Swedish Snus is not a
6 * * risk factor for periodontal disease and has fewer
adverse effects than tobacco40–42. Swedish Match has
MEAN VALUES

5 also recently filed an application with the US Food

4 and Drug Administration (FDA) to market their pro-
duct in the USA on the basis of their claims41,42.
3 In many countries in South East Asia, including
2 India, over 90% of smokeless tobacco users add betal
quid mixture to the tobacco (Gutkha)43.This makes
1
this population more susceptible to periodontal dis-
0 ease because the betel quid mixture has been known
Plaque
Index
Debris
Index
Calculus
Index
Gingival
Inflammaon
Probing
Depth
to aggravate the effects of tobacco43. In the current
PERIODONTAL PARAMETERS
study, we found Gutkha (69.47%) to be the most
commonly used smokeless tobacco form in the sub-
Figure 1. Periodontal parameters. Overview of the interrelationship of jects assessed, followed by creamy snuff (30.53%) (a
periodontal parameters amongst the three groups [smokeless tobacco paste consisting of tobacco, clove oil, glycerin, spear-
(ST; n = 121), smoking (SG; n = 81) and no tobacco (NT; n = 84). The
association of tobacco consumption and smoking with the periodontal mint, menthol and camphor in a toothpaste tube;
risk indicators was measured using analysis of variance (ANOVA). locally known as Mishri in South East Asia). Unlike
Values represent mean score  standard deviation. *Plaque Index cigarette smokers, who develop widespread periodontal
(P≤0.05) and Calculus Index (P ≤ 0.01) scores were statistically signifi-
cant. Debris Index and Periodontal Disease Index (gingival inflammation destruction, the effects of smokeless tobacco can be
and probing depth) scores were not statistically significant but showed a localised to the placement site in the mouth44 The fore-
tendency to be higher in ST and SG groups than in the most periodontal change is localised gingival recession
NT group.
(occurring in 25–30% of these users)44. Acute necrotis-
ing ulcerative gingivitis (ANUG) has also been noted to
total number of patients consumed tobacco in either occur with chronic tobacco consumption44. However,
smokeless or smoking form. The majority of subjects in in our study, we did not find any cases that were just
the SG and ST groups stated that they turned to localised; most had periodontal involvement, which
tobacco use to deal with problems, such as depression, was quite generalised in nature.
because of their low standard of living and low income. Some shortcomings need to be considered when
In the present study, a link between tobacco con- interpreting the data presented in this study. As a
sumption (SG and ST groups) and periodontal disease result of limited availability of resources (no X-ray
markers was established, supporting previous research facility to determine the level of alveolar bone
data4,36. Moreover, previous studies28,37 have demon- destruction, hesitance of people to participate in the
strated greater calculus deposits in smokers37, survey, and time constraints), these findings may not
although the level of plaque can be variable28. Smok- be representative of the entire rural population of
ers also tend to show decreased gingival inflammation Virar. We were not able to substantiate the self-re-
as the signs of gingivitis become masked as a result of ported tobacco use of patients. Also, due to the
aberrant neutrophil function and localised vasocon- design, this study does not correlate the severity of
striction29. periodontitis with an increase or decrease in the
Clinical evaluation of smokers demonstrated quantity of tobacco consumed over a specified period
delayed periodontal healing and increased incidence of time. We chose to use the PDI rather than the
of attachment loss5,38,39. This was also evident in a 6- plaque index (PI) and Community Periodontal Index
year longitudinal study, in which smokers had 50% of Treatment Needs (CPITN). The PDI has been
less improvement in probing depth and CAL than shown to be sensitive, and more accurate than the PI
non-smokers32. In our study, although we did not find and CPITN in longitudinal trials, in assessing the
a statistically significant difference between the PD for periodontal status of an individual person45. How-
the ST and SG groups, the ST group had a higher ever, the PDI is not used as frequently as other peri-
mean value. The ST group also had a high percentage odontal indices as it considers periodontitis to be an
of patients with BOP, indicating the presence of extended version of gingivitis and does not treat both
inflammation. Furthermore, the ST group had a statis- as two separate diseases.
tically significantly higher PI compared with both SG Despite the limitations arising from the collected data
and NT groups. We can thus surmise that the ST (partial recording because of the use of Ramfjord teeth)
group had similar levels of periodontal inflammation and the cross-sectional study design, our results might
as the SG group. Interestingly, ‘Swedish Snus’ (a be an important guide to direct future research on
smokeless tobacco) is classified as a Modified Risk the link between smokeless tobacco and periodontal
© 2015 FDI World Dental Federation 33
Kulkarni et al.

disease. The results obtained in this study can be used Conflict of interest
by clinicians to highlight the detrimental effect of
None.
smokeless tobacco and to dispel the growing belief
amongst patients that smokeless tobacco is safer to use
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