Indian Journal of Dental ResearchIndian Journal of Dental ResearchIndian Journal of Dental Research
HOME | ABOUT US | EDITORIAL BOARD | AHEAD OF PRINT | CURRENT ISSUE | ARCHIVES | INSTRUCTIONS | SUBSCRIBE | ADVERTISE | CONTACT
Indian Journal of Dental Research   Login   |  Users online: 259

Home Bookmark this page Print this page Email this page Small font sizeDefault font size Increase font size         

 


 
Table of Contents   
ORIGINAL RESEARCH  
Year : 2020  |  Volume : 31  |  Issue : 3  |  Page : 433-438
Effect of bidi cigarette smoking on interleukin-1β and 8 levels in chronic periodontitis patient


1 Department of Dentistry, Rajendra Institute of Medical Sciences, Ranchi, Jharkhand, India
2 Senior Lecturer, Hazaribagh College of Dental Sciences and Hospital, Hazaribagh, Jharkhand, India
3 Department of Restorative Dentistry, School of Dentistry, International Medical University, Kuala Lumpur, Malaysia

Click here for correspondence address and email

Date of Submission29-Dec-2017
Date of Decision26-Jun-2019
Date of Acceptance29-Oct-2019
Date of Web Publication06-Aug-2020
 

   Abstract 


Introduction: Bidi, a leaf rolled cigarette, is the most popular form of smoking in India. Bidi cigarette contains higher tar, ammonia, and nicotine content than a conventional cigarette and is more hazardous. Aim of Study: The aim of this study was to determine the effect of bidi smoking on periodontitis by assessing the interleukin (IL)-1β and IL-8 from a gingival crevicular fluid (GCF). Materials and Methods: A total of 60 patients were selected, which included 40 patients diagnosed with chronic periodontitis (20 bidi smokers and 20 non-bidi smokers) and 20 periodontal healthy controls. Diseased and healthy sites were selected from each of the chronic periodontitis subjects. Clinical parameters assessed were plaque index (PI), gingival index (GI), periodontal probing depth (PPD), recession (RC), and clinical attachment level (CAL). Pooled GCF samples were taken from the same site and analyzed for IL-1β and IL-8 using enzyme-linked immunosorbent assay. Results: Bidi smokers displayed decreased levels of IL-1β and IL-8 than non-bidi smokers for both healthy and diseased sites and significantly reduced IL-8 levels among bidi smokers when compared to controls. Among bidi smokers, the diseased site had significantly higher levels of IL-8 than the healthy site. Non-smoker subjects with chronic periodontitis especially diseased sites contained significantly higher amounts of IL-1β and IL-8 than smokers and controls. The PI scores were highest among bidi smokers with reduced BOP and GI scores. Conclusions: Bidi smoking influenced the cytokine profile among periodontitis patients exhibiting decreased levels of IL-1β and IL-8.

Keywords: Cytokines, gingival crevicular fluid, interleukin-8, interleukin -1β, periodontitis, smoking

How to cite this article:
Nath S, Prakash J, Prajapati VK, Sharma N, Pulikkotil SJ. Effect of bidi cigarette smoking on interleukin-1β and 8 levels in chronic periodontitis patient. Indian J Dent Res 2020;31:433-8

How to cite this URL:
Nath S, Prakash J, Prajapati VK, Sharma N, Pulikkotil SJ. Effect of bidi cigarette smoking on interleukin-1β and 8 levels in chronic periodontitis patient. Indian J Dent Res [serial online] 2020 [cited 2020 Sep 18];31:433-8. Available from: http://www.ijdr.in/text.asp?2020/31/3/433/291499



   Introduction Top


Smoking is regarded as one of the most significant risk factors in the pathogenesis and progression of periodontal disease.[1],[2] Smoking has a significant impact on the rate of plaque accumulation and the severity of periodontal disease. Investigators have shown that smokers have greater loss of clinical attachment, alveolar bone loss and deep periodontal pockets, tooth loss, and a poor response to periodontal therapy when compared with non-smokers.[3],[4] The role of cigarette smoking in the pathogenesis of periodontal disease has been extensively studied and well documented by several investigators. However, less is known about the periodontal effects of non-cigarette smoking product, such as bidi.

India is one of the world's highest tobacco consumers.[5] Approximately, 19% of tobacco consumption in India is in the form of cigarettes, of which 53% are bidi smokers. Bidi is most popular in India especially in rural areas and populations of low socioeconomic status.[5] Bidis are also exported abroad to about 122 countries and have become popular especially in the United States among youngsters as a safer alternative to conventional cigarette.[5]

Bidis are slim, leaf rolled unfiltered cigarettes. The bidi contains 0.2 g of sun-dried course and processed tobacco flakes rolled in tendu leaf (diospyroselanoxylon) or temburni leaf (diospyrosmelanoxylon) and tied with a cotton string at one end.[6] Bidi is more hazardous than conventional cigarette, and bidi contains one-fourth the quantity of tobacco.[7] The mainstream smoke of bidi contains a higher concentration of toxic agents such as hydrogen cyanide, carbon monoxide, ammonia, other volatile phenols, and carcinogenic hydrocarbons such as benz(a) anthracene and benzopyrene. Bidi smoking, when compared to conventional cigarette smoking, delivers 3–5 times more nicotine, tar, and carbon monoxide.[7],[8] A study report showed bidi contains 1.5 times more carcinogenic hydrocarbons than American cigarettes.[9] Bidi smokers have to take at least five puffs in a minute compared to two puffs of cigarette smoking to keep the cigarette lit. Several studies have proved that bidi smokers are at higher risk for lung cancer, oral cancer, gastric cancer, ischemic heart disease than a conventional cigarette smoker.[6],[10],[11]

The mechanism by which smoking may cause periodontal destruction are two-fold; alteration in the subgingival microbial flora and affecting the immune system by impairing the chemotaxis and/or phagocytosis of neutrophils leading to modification in the production of cytokines or inflammatory mediators.[12] It is likely that interactions between nicotine and bacteria may result in enhanced pro inflammatory cytokine production contributing to increased periodontal destruction among smokers.[12],[13] The research conducted has shown conflicting results regarding the influence of smoking on pro-inflammatory cytokines and chemokines.[14],[15],[16],[17] Although a number of studies have considered smoking as a true risk factor for periodontitis, the mechanism is still unclear because of varying results.[18]

Bidi is considered as poor man's cigarette because a large number of patients in rural India are bidi users instead of cigarette users. All forms of tobacco products (hookah, chutta, chillum, and bidi) have a variable effect on the periodontium. Therefore, it becomes prudent to study the effect of bidi smoking on periodontal health. We hypothesized that bidi smoking would result in enhanced pro-inflammatory cytokine production, which may lead to increased periodontal destruction. To understand the pathogenesis, there is abundant data on conventional cigarette smoking assessing different cytokines and chemokine but no documented reports showing the effect of bidi smoking on periodontal inflammation.[18] Moreover, to our knowledge, no study to date has been done to evaluate the effects of bidi smoking on gingival crevicular fluid (GCF) pro-inflammatory cytokines. Therefore, the aim of this study was to evaluate the influence of bidi smoking on GCF IL-1β and IL-8 levels in patients with chronic periodontitis.


   Materials and Methods Top


This was a cross-sectional study designed to evaluate the effects of bidi smoking in chronic periodontitis patients. The study was conducted in the Department of Dentistry, Rajendra Institute of Medical Sciences, Ranchi, India after obtaining approval from the Institutional Review Board. The study was conducted from September 2016 to February 2017. The nature of the study was explained in detail, and written informed consent was taken from every patient who decided to participate in the study.

Study participant

A total of 60 subjects were selected for this study, which included 40 patients with chronic periodontitis (20 bidi smokers and 20 non bidi smokers) and 20 periodontally healthy controls (HC). Periodontally, diseased subjects had a diagnosis of generalized severe chronic periodontitis (>30% of sites with a clinical attachment level and periodontal probing depth ≥5 mm). Bidi smokers (n = 20) were defined as subjects who smoked ≥10 bidi daily for ≥5 years, and non-smokers (n = 20) were those who reported to have not smoked any form of tobacco, either conventional cigarette or bidi for the past 10 years. Subjects who had clinically healthy gingiva and PD ≤3 mm were included in HC group.

Patients were excluded for the following conditions:(1) age range was <25 or >55 years; (2) subjects had <22 permanent teeth; (3) taking any type of medication chronically or in the last 2 weeks; (4) having any given chronic medical condition, including diabetes and viral, fungal, or bacterial infections; (5) having any type of medical condition in the last 2 weeks, including flu, upper respiratory infection, allergy, skin disorders, and sinus problem; (6) having aggressive periodontitis, periodontal abscess, or necrotizing ulcerative gingivitis; (7) received periodontal treatment and/or antibiotic therapy within the preceding 3 months; (8) subjects who had any type of dental work or tooth extraction (s) in the last 2 weeks; (9) having carious lesions; (10) former smokers; and (11) subjects who refused to sign the consent form.

Site selection

Five sites having the disease [periodontal probing depth (PPD) and clinical attachment level (CAL) ≥5 mm] and five healthy sites [PD ≤3 mm, absence of recession (RC), and bleeding] were selected from each patient in chronic periodontitis group (N = 40). The healthy and diseased sites in the 20 bidi smokers were identified as bidi smoker healthy sites (BH) and bidi smoker disease sites (BD), respectively. In the 20 non-smokers, the healthy and diseased sites were designated as non smoker healthy sites (NH) and non smoker disease sites (ND), respectively. Five sites from HC group were selected. From each of the five selected sites (BH, BD, NH, ND, and HC), clinical assessment and collection of GCF for volume, and interleukin assessment was done.

Periodontal examination

The clinical and periodontal examination was carried out by a single calibrated periodontist (S.N) and recorded by another dentist (J.P). The clinical examination included assessment of plaque index (PI),[19] gingival index (GI),[20] bleeding on probing (BOP), probing pocket depth, gingival RC, and CAL. The BOP was recorded as overall percentage of sites with bleeding occurring within 15 s of probing. PPD was defined as the distance in millimeter from the most coronal margin of the free gingiva to the most apical penetration of the probe. CAL was defined as the distance in millimeter from the cementoenamel junction to the most apical point of penetration of the probe. All the measurements were made on six sites per tooth (distobuccal, buccal, mesiobuccal, mesiolingual, lingual, and distolingual) and carried out using UNC-15 periodontal probe (Hu-Friedy Inc. ®, Chicago, Illinois, USA).

Examiner calibration

A single periodontist (SN) was trained and calibrated prior to the start of the study. The GI and PI was assessed on 10 random sites and then reassessed again after 60 min. The interclass correlation coefficient was used for assessing the examiner's repeatability score. The mean interclass coefficient was 0.89 and 0.92 for GI and PI, respectively.

GCF sampling

GCF collection was carried out 1 week after clinical measurements were recorded. GCF collection was done from the five pre-selected sites, the deepest one in each quadrant. The teeth were air-dried and isolated with cotton rolls, and the supragingival plaque was gently removed. The 1–5 μl calibrated microcapillary pipettes (Sigma Aldrich Chemical Co®., St. Louis, MO, USA) were used for GCF sample collection by placing them extra-crevicularly. In case of visible contamination with blood, the microcapillary pipettes were discarded and another site fulfilling the same criteria was selected.

Analysis of interleukin

A commercially available sandwich enzyme-linked immunosorbent assay (ELISA) kit (Raybio®, Human Elisa kits, RayBiotech, Inc., USA) was used for the assessment of IL-1β and IL-8 from GCF sample. The assays were performed according to manufacturer's instructions using human recombinant standards. Each sample was assayed in duplicate. The level of cytokine expression was assessed by an ELISA reader at 450 nm. The concentration of the IL-1β and IL-8 were reported as pictogram per milliliter of the sample (pg/mL).

Statistical analysis

The demographic characteristics such as age and bidi used per day were described using mean ± standard deviation (SD). Analysis of normality and non-parametric test were used based on the distribution of data. Intergroup comparison for PI, GI, BOP, PPD, RC and CAL was done using the Mann-Whitney test. For GCF volume and cytokines levels of pooled healthy and diseased sites among bidi smokers and non smokers and controls were compared using the Mann-Whitney test. Matched healthy and diseased sites for each group were compared. Wilcoxon signed-rank test was used for intragroup comparison between matched healthy and disease sites for bidi smokers, non smoker, and control group. The significance level was set at 5%. SPSS software (Version 19.0, SPSS Inc., Chicago, IL, USA) was used for data entry and analysis.


   Results Top


Patient biographical and clinical data

The patient's biographical data such as mean age, sex, and bidi smoking habit are described under [Table 1]. There were more number of males than females (17:3) in the bidi smoker group, 11:9 in chronic periodontitis group, and 10:10 in HC group. The PI scores were significantly higher in bidi smokers than non-bidi smokers. However, the GI and BOP scores were lesser among bidi smokers. When HC group was compared to the chronic periodontitis group (bidi smoker and non smoker), the difference for GI, PI, and BOP scores was significant. [Table 2] describes the periodontal status of healthy and disease sites among all three groups. A significant difference was observed for PPD, RC, and CAL (P < 0.001) when BH/BD and NH/ND were compared. In an intergroup comparison of CAL, the values were significant when BH/NH (0.03) and BH/HC (0.006) were compared [Table 3]. There were no significant changes present for PPD and RC in any intergroup comparisons.
Table 1: Demographic characteristics of population

Click here to view
Table 2: Site characteristic and intragroup comparison between healthy and disease site

Click here to view
Table 3: P value of intergroup comparison of clinical parameters and cytokine levels

Click here to view


GCF Interleukin levels

The intragroup analysis between healthy and disease sites among bidi smokers and non smokers is described under [Table 4]. The P value of intergroup comparison is described under [Table 3]. The GCF volume was statistically significant (P = 0.001) when NH and ND were compared and BH had more GCF volume than NH (P = 0.05) sites. In intragroup analysis, the non smokers diseased sites had significantly higher levels of both IL-1β and IL-8 (P = 0.04, 0.03) when compared to healthy sites, whereas among bidi smokers only IL-8 levels were significantly higher (P = 0.001) for the diseased site. When matched comparison was done among healthy and diseased sites of bidi smoker and non smoker, a significant difference was observed for IL-1β and IL-8 levels (P < 0.001). Non smokers with chronic periodontitis had an increase in both IL-1β and IL-8 (P < 0.001, 0.006) when compared with HC, whereas bidi smokers showed a significant difference in IL-8 (P < 0.001).
Table 4: P value of intragroup analysis of cytokines level

Click here to view



   Discussion Top


To our knowledge, there is no documented report explaining the mechanism of periodontal destruction among bidi smokers suffering from periodontitis. Although there is abundant report on cigarette smoking, our study was conducted to explain the role of bidi smoking in pathogenesis and progression of periodontal disease by assessing the inflammatory cytokines from GCF.

The common forms of smoking tobacco include cigarettes, bidi (tobacco rolled in a leaf and tied with string on one end), chutta (coarsely prepared cheerot, lighted end is placed in mouth), and hookah (tobacco kept in an earthen pot and smoked through a water container).[21] Little information is available regarding the use of bidi among rural population of Jharkhand where both poor oral hygiene and severe periodontitis are common finding. Bidi smoking is the most popular form of smoked tobacco, and it is considered as the poor man's cigarette; it is cheaper and smaller than conventional cigarettes.[5],[22] In our study, the average bidi smoker consumed 45.5 ± 12.5 in a day. A relationship has been demonstrated between the prevalence of moderate to severe periodontal disease and the number of cigarettes smoked per day.[23] There were a greater number of males among bidi smokers than in any other group.

In our study, the PI is significantly higher in bidi smokers than non smoker and least in the control group. In spite of high plaque scores, the GI and BOP were lower among bidi smokers than non-smoker group. A direct comparison was not possible due to lack of studies on bidi smoking. Bidi smokes showed similar clinical effects compared to conventional cigarette smoking. According to Bergstrom and Preber,[24] smokers do not develop gingivitis to greater extent than non smokers with the same level of oral hygiene. A number of studies have confirmed that gingivitis expression in response to dental plaque is modified in smoking. In spite of having increased plaque accumulation among smokers, the gingival bleeding and inflammation are reduced.[25] Smoking tends to mask gingival inflammation by causing constriction of the blood vessel.[25],[26],[27] Nicotine has a vasoconstrictive effect causing a reduction in gingival blood flow.[27]

Cytokines are involved in both inflammation-related alteration and repair of the periodontal tissues. Certain cytokines have been proposed as potentially useful diagnostic or prognostic marker of destruction,[2],[12],[14] and GCF can be used as medium for this detection of these inflammatory mediators.[11],[12] Altered cytokine production is one of the explanations of smoking-related periodontal destruction. IL-1β is a multifunctional inflammatory mediator able to modulate bone resorption by the activation of osteoclast and by stimulating prostaglandin E2 synthesis.[3] IL-8 plays a key role in the accumulation of leukocytes at the sites of inflammation and increased level is seen in inflamed site.[9] Gingival keratinocytes are the first cells to be in contact with numerous chemical present in tobacco product and are early producers of cytokines and chemokines, including IL-1 and IL-8 in response to bacterial plaque. Abundant information is available regarding cigarette smoking but little information regarding effect of bidi smoking on inflammatory cytokine.[1]

Bidi smokers suffering from periodontitis have a lowered level of IL-1β when compared to non smoker but similar to healthy control. Bidi smoking brings the IL-1β level down to healthy level irrespective of healthy and diseased site. The lowered IL-1 levels are in agreement with other studies[14],[27] while Bostrom et al.[3] revealed no influence of smoking on IL-1β and IL-1ra. The IL-8 levels of bidi smoker healthy sites are 3 times less than healthy controls and six times less than non-smoker healthy site. The IL-8 levels among diseased site of bidi smoker are six times less than that of diseased site on non-bidi smoker. When healthy and diseased sites are compared increased IL-8 levels were seen in diseased site among bidi smokers. The differences in the interleukin level may be because of the differences in nicotine content in bidi and also the ability of the host to maintain a balance between the proinflammatory and other regulatory cytokines. Nicotine, the major component is present as high as 26.9–37.7 mg/gm in bidi, whereas cigarette contains 15 mg/gm.[4],[7],[28] Some studies reported that nicotine either suppresses or has no effect on proinflammatory cytokines.[9],[13],[14],[29] Another possible explanation is that there a general reduction in inflammation in smokers, reduced number of neutrophils in GCF resulting in decreased total local or a direct suppression of cytokine production.[14]

Among non smokers having chronic periodontitis, both IL-1β and -8 levels were significantly raised irrespective of healthy or disease site. It implies that IL1β and IL-8 is a systemic change than a localized event. It could be marker to identify a periodontitis patient than any periodontitis active or non-active site. Similar findings were seen by others researchers,[28],[30] where periodontitis causes increased levels of inflammatory cytokine. The GCF volume was more in diseased sites of both bidi smokers and non-smokers. Matched healthy sites showed more GCF volume for bidi smokers than non smoker. The collection of GCF was similar to the method described by the authors earlier.[31] Other studies have shown smoking to produce an immediate transient but marked increase in gingival fluid flow,[32],[33] whereas Kinane and Radvar[34] have found lower GCF volume for smokers than non-smokers.

Effective strategies are now needed to expand the focus on to all types of tobacco products including usage of bidi. Tobacco control programs should incorporate the harmful effects of bidi smoking in their mix of intervention like, controlled production of bidi, health warnings on the packets, and high taxes.

A major limitation of our study is the cross-sectional study design that makes it impossible to observe the time course of the events; hence, it is difficult to infer causal relations. The clinical examination was carried out in a standard way, but investigators could not be blinded as to the exposure status of the participants.


   Conclusion Top


The important finding in our study was that bidi smoking might have influenced the cytokine levels causing a decrease in levels of IL-1β and IL-8. The IL-8 levels among bidi smokers were even lower than healthy controls. The findings suggest that bidi smoking affects the inflammatory mechanism causing reductions in levels of cytokine. Further studies are required to investigate the influence of bidi smoking on all involved cytokine level. Longitudinal studies should be conducted among smokers with extended follow-up, and the influence of periodontal treatment on the cytokine levels should be studied.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form, the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Palmer RM, Wilson RF, Hasan AS, Scott DA. Mechanisms of action of environmentalfactors – tobacco smoking. J Clin Peridontol 2005;32(Suppl 6):180-95.  Back to cited text no. 1
    
2.
Tymkiw KD, Thunell DH, Johnson GK, Joly S, BurnellKK, Cavanaugh JE, et al. Influence of smoking on gingival crevicular fluid cytokines in severe chronic periodontitis. J Clin Periodontol 2011;38:219-28.  Back to cited text no. 2
    
3.
Bostrom L, Linder LE, Bergstrom J. Smoking and GCF levels of IL-1β and IL- 1ra in periodontal disease. J Clin Periodontol 2000;27:250-5.  Back to cited text no. 3
    
4.
Reddy SS, Ali SHKH. Estimation of nicotine content in popular Indian brands of smoking and chewing tobacco products. Indian J Dent Res 2008;19:88-91.  Back to cited text no. 4
[PUBMED]  [Full text]  
5.
Bidi Smoking and Public Health. World Health Organization, March 2008. Available from: www.who.int/tobacco/publications/prod_regulation/bidi_smoking_public_health.pdf. [Last accessed on 2018 Nov 24].  Back to cited text no. 5
    
6.
Rahman M, Sakamoto J, Fukui T. Bidi smoking and oral cancer: A meta-analysis. Int J Cancer 2003;106:600–4.  Back to cited text no. 6
    
7.
Prasad R, Singhal S, Garg R. Bidi smoking and lung cancer. Biosci Trends 2009;3:41-3.  Back to cited text no. 7
    
8.
MalsonJL, Sims K, Murty R, Pickworth WB. Comparison of the nicotine content of tobacco used in bidis and conventional cigarettes. Tob Control 2001;10:181-3.  Back to cited text no. 8
    
9.
Hoffman D, Sanghvi LD, Wynder EL. Comparative chemical analysis of Indian bidi and American cigarette smoke. Int J Cancer 1974;14:49-55.  Back to cited text no. 9
    
10.
Jayalekshmi PA, Hassani S, Nandakumar A, Koriyama C, Sebastian P, Akiba S. Gastric cancer risk in relation to tobacco use and alcohol drinking in Kerala, India--Karunagappally cohort study. World J Gastroenterol 2015;21:12676-85.  Back to cited text no. 10
    
11.
Wu F, Chen Y, Parvez F, Segers S, Argos M, Islam T, et al. A prospective study of tobacco smoking and mortality in Bangladesh. PLoS One 2013;8:e58516.  Back to cited text no. 11
    
12.
Johnson GK, Guthmiller JM, Joly S, Organ CC, Dawson DV. Interleukin-1 and interleukin-8 in nicotine- and lipopolysaccharide-exposed gingival keratinocyte cultures. J Periodont Res 2010;45:583-8.  Back to cited text no. 12
    
13.
Payne JB, Johnson GK, Reinhardt RA, Dyer JK, Maze CA, Dunning DG. Nicotine effects on PGE2 and IL-1 beta release by LPS-treated human monocytes. J Periodontal Res 1996;31:99-104.  Back to cited text no. 13
    
14.
ErdemirEO, Duran I, Haliloglu S. Effects of smoking on clinical parameters and the gingival crevicular fluid levels of IL-6 and TNF-alpha in patients with chronic periodontitis. J Clin Periodontol 2004;31:99-104.  Back to cited text no. 14
    
15.
Giannopoulou C, KammaJJ, Mombelli A. Effect of inflammation, smoking and stress on gingival crevicular fluid cytokine level. J Clin Periodontol 2003;30:145-53.  Back to cited text no. 15
    
16.
Rawlinson A, GrummittJM, Walsh TF, Ian Douglas CW. Interleukin 1 and receptor antagonist levels in gingival crevicular fluid in heavy smokers versus non-smokers. J Clin Periodontol 2003;30:42-8.  Back to cited text no. 16
    
17.
Petropoulos G, McKay IJ, Hughes FJ. The association between neutrophil numbers and interleukin-1alpha concentrations in gingival crevicular fluid of smokers and non-smokers with periodontal disease. J Clin Periodontol 2004;31:390-5.  Back to cited text no. 17
    
18.
César Neto JB1, Rosa EF, Pannuti CM, Romito GA. Smoking and periodontal tissues: A review. Braz Oral Res 2012;26:25-31.  Back to cited text no. 18
    
19.
Silness J, Loe H. Periodontal disease in pregnancy. II. Correlation between oral hygiene and periodontal condition. Acta OdontolScand 1964;22:121-35.  Back to cited text no. 19
    
20.
Loe H, Silness J. Periodontal Disease in Pregnancy. I. Prevalence and Severity. Acta OdontolScand 1963;21:533-51.  Back to cited text no. 20
    
21.
Anand PS, Kamath KP, Shekar BR, Anil S. Relationship of smoking and smokeless tobacco use to tooth loss in a central Indian population. Oral Health Prev Dent 2012;10:243-52.  Back to cited text no. 21
    
22.
MalsonJL, Pickworth WB. Bidis--hand-rolled, Indian cigarettes: Effects on physiological, biochemical and subjective measures. PharmacolBiochemBehav 2002;72:443-7.  Back to cited text no. 22
    
23.
Salem A, Hilow H, Khraisat A, Smadi L, Ryalat S. Association between intensity of smoking and periodontal pockets among young university students. Odontostomatol Trop 2008;31:5-10.  Back to cited text no. 23
    
24.
Bergström J, Preber H. Tobacco use as a risk factor. J Periodontol 1994;65 (5 Suppl):545-50.  Back to cited text no. 24
    
25.
Bergström J. Oral hygiene compliance and gingivitis expression in cigarette smokers. Scand J Dent Res 1990;98:497-503.  Back to cited text no. 25
    
26.
Ustün K, Alptekin NO. The effect of tobacco smoking on gingival crevicular fluid volume. Eur J Dent 2007;1:236-9.  Back to cited text no. 26
    
27.
McLaughlin WS, Lovat FM, Macgregor IDM, Kelly PJ. The immediate effects of smoking on gingival fluid flow. J Clin Periodontol 1993;20:448-51.  Back to cited text no. 27
    
28.
Pakhale SS, Maru GB. Distribution of major and minor alkaloids in tobacco, mainstream and sidestream smoke of popular Indian smoking products. Food Chem Toxicol 1998;36:1131-8.  Back to cited text no. 28
    
29.
de Heens GL, Kikkert R, Aarden LA, van der Velden U, Loos BG. Effects of smoking on the ex vivo cytokine production in periodontitis. J Periodontal Res 2009;44:28-34.  Back to cited text no. 29
    
30.
Deo V, Bhongade ML. Pathogenesis of periodontitis: Role of cytokines in host response. Dent Today 2010;29:60-2, 64-6; quiz 68-9.  Back to cited text no. 30
    
31.
Jacob PS, Nath S, Patel RP. Evaluation of interleukin-1β and 8 in gutka chewers with periodontitis among a rural Indian population. J Periodontal Implant Sci 2014;44:126-33.  Back to cited text no. 31
    
32.
Mavropulos A, Aars H, Brodin P. Hyperamic response to cigarette smoking in healthy gingiva. J Clin Periodontol 2003;30:214-21.  Back to cited text no. 32
    
33.
Morozumi T, Kubota T, Sato T, Okuda K, Yoshie H. Smoking cessation increases gingival blood flow and gingival crevicular fluid. J Clin Periodontol 2004;31:267-72.  Back to cited text no. 33
    
34.
Kinane DF, Radvar M. The effect of smoking on mechanical and antimicrobial periodontal therapy. J Periodontol 1997;68:467-72.  Back to cited text no. 34
    

Top
Correspondence Address:
Dr. Sonia Nath
Rajendra Institute of Medical Sciences, Department of Dentistry, Ranchi - 834 009, Jharkhand
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijdr.IJDR_783_17

Rights and Permissions



 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

Top
 
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Email Alert *
    Add to My List *
* Registration required (free)  
 


    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
   Conclusion
    References
    Article Tables

 Article Access Statistics
    Viewed114    
    Printed1    
    Emailed0    
    PDF Downloaded12    
    Comments [Add]    

Recommend this journal