Indian Journal of Dental Research

: 2021  |  Volume : 32  |  Issue : 1  |  Page : 15--22

Comparative evaluation of periodontal inflammatory conditions among gutka-chewers with and without prediabetes

Puneet Bhardwaj1, Zoya Chowdhary2, Vandana Sharma3, Ravi Ladani4, Sonamben Kishorchandra Modi5, Sudhanshu Bhardwaj6, Kasper D Hundal7,  
1 Department of Dentistry, Jawaharlal Nehru Medical College, Ajmer, Rajasthan, India
2 Department of Periodontology, Indira Gandhi Government Dental College, Jammu, J and K, India
3 Periodontist, Private Practitioner, Oral Solutions, Ajmer, Rajasthan, India
4 Periodontist, Private Practitioner, Family Dental Care, Rajkot, Gujrat, India
5 Periodontist, Private Practitioner, Handa's Multispeciality Dental Clinic, Hazaribagh, Jharkhand, India
6 Periodontist, Private Practitioner, Clove Dental, Jaipur, Rajasthan, India
7 Department of Oral Medicine and Radiology, Daswani Dental College and Research Centre, Kota, Rajasthan, India

Correspondence Address:
Zoya Chowdhary
Department of Periodontology, Indira Gandhi Government Dental College, Jammu, J and K


Background: The metabolic syndrome has become one of the major public-health challenges worldwide which include diabetes, prediabetes (raised blood glucose level), abdominal obesity, high cholesterol level, and high blood pressure. Periodontitis is described as a multi-factorial irreversible and cumulative condition and, is also the sixth complication of diabetes. Areca nut chewing has already been linked with the development of various cancers, and more recently with metabolic syndrome. Therefore, the purpose of the study is to investigate the association of periodontal inflammatory conditions among gutka chewing with and without prediabetes patients. Materials and Methods: There are about 50 pre-diabetic and 50 healthy patients, both males and females with the age range of 18 years to 45 years, were included in the study. They were then divided into 4 groups based upon gutka chewers and non-chewers i.e., pre-diabetic gutka chewers (PDC), pre-diabetic non-chewers (PDNC), healthy gutka chewers (HC), and healthy non-chewers (HNC). A complete demographic data was obtained along with clinical and radiographic parameters i.e. plaque index (PI), sulcus bleeding index (SBI), probing depth (PD), marginal bone loss (MBL) were recorded. A statistical analysis was performed and Bonferroni adjustment post hoc test was performed for multiple comparisons. Results: The overall results suggested that the clinical periodontal parameters i.e., PD, PI, SBI and radiologic parameters i.e., MBL are significantly higher in prediabetes chewers compared with healthy chewers and healthy non chewers. Conclusion: The periodontal inflammatory conditions are worse in gutka chewers compared to non-chewers in healthy and pre-diabetic patients, concluding that the severity of periodontal inflammation is governed by hyperglycemia when compared to habitual gutka usage.

How to cite this article:
Bhardwaj P, Chowdhary Z, Sharma V, Ladani R, Modi SK, Bhardwaj S, Hundal KD. Comparative evaluation of periodontal inflammatory conditions among gutka-chewers with and without prediabetes.Indian J Dent Res 2021;32:15-22

How to cite this URL:
Bhardwaj P, Chowdhary Z, Sharma V, Ladani R, Modi SK, Bhardwaj S, Hundal KD. Comparative evaluation of periodontal inflammatory conditions among gutka-chewers with and without prediabetes. Indian J Dent Res [serial online] 2021 [cited 2021 Aug 3 ];32:15-22
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Periodontitis is one of the most common oral diseases and is characterized by gingival inflammation and alveolar bone resorption.[1] It is described as a multi-factorial irreversible and cumulative condition, initiated and propagated by bacteria, and host factors.[2]

The metabolic syndrome has become one of the major public-health challenges worldwide. The metabolic syndrome is defined as a cluster of dangerous risk factors (particularly for heart disease), which include diabetes, prediabetes (raised blood glucose level), abdominal obesity, high cholesterol level and high blood pressure. Recently, areca nut chewing has been linked with metabolic syndrome and it has been estimated that approximately 600 million individuals chew areca nut worldwide making it fourth commonest substance after nicotine, ethanol and caffeine.[3]

Periodontitis is much more than a localized oral infection. The interrelationship between the periodontitis and diabetes suggests the predisposition of systemic disease to oral infection and vice versa.[4] Despite being extensive research, mechanism underlying the association of periodontitis and diabetes mellitus is not clear.

Due to the accumulation of dental plaque, an inflammatory reaction occurs in the gingiva leading to clinical attachment loss, gingival enlargement or recession, loss of alveolar bone, and periodontal pocket formation, or bleeding gums in susceptible individuals, and if remain untreated ultimately results into tooth loss.[5] However, in case of diabetic patients, concentration of oral microbial flora is increased due to higher concentration of glucose in saliva and crevicular fluid. Periodontal disease has been suggested as the ''Sixth complication of diabetes”.[6] Diabetes is an important risk factor for periodontal inflammation,[7],[8] and severity of periodontal inflammatory parameters varies depending on the maintenance of blood glucose levels.[9]

Diabetes mellitus is a systemic disease with several major complications affecting both the quality and length of life. Studies have reported that periodontal inflammatory parameters and marginal bone loss (MBL) are worse in patients with poorly controlled diabetes compared with healthy controls.[10],[11],[12] In addition, it has been reported that patients with impaired glucose tolerance (prediabetes) demonstrated more severe periodontal inflammatory parameters than healthy individuals.[13] Although the exact mechanism through which hyperglycemia (in patients with diabetes and prediabetes) promotes periodontal inflammation remains unclear. It has been proposed that an interaction between the advanced glycation end products (AGEs), and their receptors (RAGs) produced as a result of hypergylcemia in the periodontal tissues impairs the chemotactic and phagocytic function of polymorphonuclear leukocytes and produces proinflammatory cytokines, thereby leading to periodontal inflammation and bone loss in these individuals.[14]

In addition, function of potential cells involved in immune inflammatory responses is impaired under chronic hyperglycemia. Manoucher-Pour et al.[15] reported that chronic hyperglycemia impairs the chemotactic and phagocytic function of neutrophils that may prevent breakdown of bacteria in periodontal pockets, thereby increasing periodontal breakdown. Prediabetes is a state of abnormal glucose homeostasis characterized by the presence of impaired fasting glucose (IFG), impaired glucose tolerance (IGT), or both. Prediabetes designations (IFG and IGT) have been defined by fasting blood glucose levels (FBGLs) of 100 to 125 mg/dL and post-glucose challenge levels of 140 to 199 mg/dL, respectively.[16] Similar to diabetes, the risk of microvascular complications is increased with prediabetes,[17] and the risk for cardiovascular disease and total mortality is almost twice as high in individuals with prediabetes.[18] Early diagnosis and intervention for prediabetes could prevent these complications, prevent delay, or prevent the transition to diabetes and be cost-effective.

Gutka is a form of smokeless tobacco that is a mixture of powdered tobacco, areca nut (fruit of the Areca catechu tree), and slaked lime (aqueous calcium hydroxide).[19] Other components of gutka include menthol and perfumery compounds such as sandalwood and musk ketones. Gutka chewing is a common practice in communities originating from south-east Asian countries including Bangladesh, India, Pakistan, and Sri Lanka etc.

Habitual gutka chewing has been associated with several oral mucosal disorders including periodontal inflammation, oral submucous fibrosis, and oral cancer.[20],[21],[22] Areca nut, an essential component of gutka, has been associated with several disorders, including epilepsy, hepatocellular carcinoma, metabolic syndrome, impaired glucose tolerance (IGT), and diabetes.[23] Slaked lime, areca nut, and powdered tobacco (the major constituents of gutka) are independent risk factors of periodontal inflammation and have also been shown to suppress the growth of cultured gingival keratinocytes and periodontal fibroblasts.[24]

Yong JC et al.[25] have also reported that arecoline has a diabetogenic effect and may result in insulin resistance by obstructing insulin signaling. The exact mechanism through which areca-nut chewing induces hyperglycemia remains debatable; however, it has been proposed that areca nut–derived nitrosamines may be diabetogenic in a way similar to streptozotocin, which targets and damages islet b-cell glucose receptors.[26]

It is known that gutka chewing produced detrimental effects on periodontal health as well as act as a diabetogenic factor by inhibiting insulin signalling and increased peripheral insulin resistance. Therefore, the aim of the present study is to investigate the severity of periodontal inflammatory conditions in gutka – chewers with and without prediabetes. In this study, it is also hypothesized that periodontal inflammatory conditions are worse in habitual gutka chewers compared with non-chewers; and severity of periodontal inflammation is higher in gutka chewers with prediabetes compared with nonchewers with prediabetes and gutka chewers without prediabetes.

 Materials and Methods

A cross-sectional study was conducted to investigate the severity of periodontal inflammatory conditions in gutka chewers with and without prediabetes. The data was obtained from the Out- patient Department of Periodontology. A total of 100 patients, both male and females, where included in the study.

Inclusion criteria

Gutka chewers – chewing at least 1 sachet of gutka per day for at least 1 year.[19]Non chewers- never consumed tobacco.Prediabetes- FBGL >100 mg/dl but <126 mg/dl.[13]Healthy controls- FBGL <100 mg/dl.

Exclusion criteria

Habitual tobacco smoking or alcohol consumption.Completely edentulous patients.Presence of other disorders including acquired immune deficiency syndrome, cardiovascular disorders, renal disease, and hepatitis B or C infection.Fractured teeth with embedded root remnants.Malocclusion (overlapping teeth).Current or recent use of corticosteroid, antibiotic, or non-steroidal anti-inflammatory medications.Third molars.

Study design

A cross-sectional study which included 100 patients, both male and females, was conducted in the Department of Periodontology to investigate the severity of periodontal inflammatory conditions in gutka chewers with and without prediabetes.

The Ethical clearance was obtained from the Institutional Ethical Committee (VDCH/EC/521). A written informed consent was obtained from the participants or their attendees before carrying out the examination which was in accordance with the World Medical Association's Declaration of Helsinki.[27]

Method of collection of data

There are about 50 patients with pre-diabetic and 50 healthy/without prediabetes were randomly selected from the routine OPD and their fasting blood glucose levels (FBGLs) were examined using glucometer (Accu-Chek Instant S Blood Glucose Monitor 1's, Roche Diabetes Care GmbH, India) by the same examiner and, were divided into two groups; Group 1: pre-diabetic group and; Group 2: without prediabetes (healthy control) according to the inclusion criteria. The groups were then further divided into gutka chewers and non-chewers. Therefore, the patients were categorized into pre-diabetic gutka chewer (PDC); healthy gutka chewers (HC); prediabetic non-gutka chewers (PDNC) and; healthy non-gutka chewers (HNC).

Both the groups were divided into three parts, i.e., Questionnaire, clinical examination and radiographic examination.


The questionnaire (contact the corresponding author) was read to the patients and answers were recorded by the examiner. It included the detailed demographic data of the patient i.e., age, sex, gutka usage, duration of gutka consumption, total duration of placement of gutka in the mouth, duration of frequency of gutka consumption in a day and also duration of placement of gutka per frequency.

Clinical examination

The clinical examination was performed after seating the patient on the dental chair. Full mouth Plaque Index (PI),[28] Sulcular Bleeding Index (SBI),[29] and Pocket Depth (PD)[30] were measured at six sites (mesio-buccal, mid-buccal, disto-buccal, distolingual/palatal, mid-lingual/palatal, and mesio-lingual/palatal) on all maxillary and mandibular teeth (excluding bilateral maxillary and mandibular third molars). SBI represented the Bleeding on Probing (BOP) of the site evaluated. PI and SBI were interpreted and an average score was calculated for each. PD was measured to the nearest millimetre with a graded probe from the gingival margin to the base of the pocket.[30]

Radiographic examination

The radiographic examination was performed after obtaining digital panoramic radiographs, which were viewed on a calibrated computer screen (Samsung SynMaster digital TV monitor) using a software program (KODAK 8000c Carestream Dental; Atlanta, GA, USA) and, Marginal bone loss (MBL) was evaluated. MBL was measured as the vertical distance from 2 mm below the cementoenamel junction (CEJ) to the most apical part of marginal bone[19] on bilateral maxillary and mandibular premolars and molars.

Statistical evaluation

Statistical analysis was performed using SPSS version 22.0 (IBM, USA); to determine whether the dependent variables (PI, BOP, PD [4 to <6 mm and ≥6 mm], and MBL) were related in a statistically significant manner with the independent variables. The independent variables were transformed into dichotomous variables, for example, gutka chewers with prediabetes versus non-chewers with prediabetes, gutka chewers without prediabetes versus non-chewers without prediabetes. The Mann Whitney U test and Kruskal Wallis test was performed for comparisons.

Odds ratios (ORs) for the risk of periodontal inflammation in gutka chewers and non-chewers with and without prediabetes were also calculated with 95% confidence intervals (CIs). Multivariable logistic regression analysis was used to calculate the OR for periodontal inflammation while simultaneously controlling for age, sex, gutka chewing, prediabetes, and (gutka × prediabetes) interaction. The P values ≤0.05 were considered statistically significant.


There are about 50 patients each of prediabetes and non-prediabetes included in the study to evaluate the association of gutka use with periodontal inflammation in total and, then within patients. Independent association of gutka use with prediabetes irrespective of periodontal inflammation was also assessed.

Out of the 100 patients, it was depicted that 75% were males and only 25% were females. The distribution of study subjects according to gender among four study groups were as follows: 19 males and 6 females in PDC, 19 males and 6 females in PDNC, 19 males and 6 females in HC, 18 males and 7 females in HNC. This shows that patients were equally distributed among all four study groups [Table 1]. The table also demonstrates that the mean age of healthy gutka chewers and non-chewers were 27.76 ± 6.91 years and 27.28 ± 7.50 years, respectively, and with prediabetes, 32.28 ± 6.79 years and 31.20 ± 8.26 years, respectively. The mean fasting blood glucose levels (FBGL) among gutka chewers with prediabetes (111.32 ± 7.67 mg/dL) was significantly higher than that in gutka chewers without prediabetes (90.48 ± 6.9 mg/dL). The non-chewers with prediabetes had significantly higher FBGL (111.92 ± 8.72 mg/dL) than gutka chewers without prediabetes (90.32 ± 8.01 mg/dL). The mean duration of gutka-chewing habits in healthy and pre-diabetics were 4.16 ± 3.09 years and 4.44 ± 3.78 years, respectively. The mean duration of placement of gutka in the oral cavity in healthy and pre-diabetics were 7.88 ± 4.81 minutes and 8.92 ± 4.60 minutes, respectively [Table 1].{Table 1}

In [Table 2], Mann Whitney U test was used to compare the durations of gutka chewing habit and gutka placement in mouth among the healthy and pre-diabetic. It demonstrated that there was no significant difference between the duration of Gutka chewing habit and duration of Gutka placement in mouth among the healthy and pre-diabetic Gutka chewers.{Table 2}

[Table 3] shows that there was a significant difference seen in the healthy and pre-diabetic gutka chewers and non-chewers when the key periodontal inflammatory parameters [PI (percentage of sites), BOP (percentage of sites), PD 4 to <6 mm (percentage of sites), PD >6 mm (percentage of sites), MBL (mm)] were measured. The mean PI (percentage of sites) value in PDC was highest (69.86) and lowest mean value was observed in HNC (25.16), respectively. The BOP (percentage of sites) represents the SBI (percentage of sites). Therefore, the mean SBI value in PDC was highest as 64.90 and lowest in HNC as 27.30. The mean PD 4 to <6 mm (percentage of sites) in PDC was highest (70.98), and lowest was observed in HNC (31.66). The mean PD >6 mm (percentage of sites) values in PDC was highest at 68.52 and lowest in HNC (30.14). The MBL (mm) mean value in PDC was highest at 65.60 and were lowest in HNC at 28.12.{Table 3}

The intergroup comparisons were made in [Table 4], and was found that there was a statistically significant difference in healthy chewers and pre-diabetic chewers; the healthy non chewers and pre-diabetic chewers and healthy non chewers and pre-diabetic non- chewers when all the key periodontal inflammatory parameters were measured.{Table 4}

Association between gutka chewing and periodontal inflammation

Overall, the Odd Ratio (OR) for periodontal inflammatory conditions in individuals with prediabetes compared to healthy controls is 9.03 (95% CI = 3.6 to 22.3) and prediabetes with and without Gutka chewing is 9.3 (95% CI = 3.2 to 26.88), chewing among individuals with prediabetes, and chewing among healthy controls did not statistically increase the odds of periodontal inflammation [Table 5].{Table 5}

Irrespective of chewing, individuals with prediabetes were 9 times more likely to have periodontal inflammation than individuals without prediabetes [Table 6]. There was no significant interaction between gutka chewing and prediabetes in relation to periodontal inflammation.{Table 6}


A cross-sectional study comprising of 100 subjects having 75 males (75%) and 25 females (25%) in the age range of 18 years to 45 years with mean age of 29.63 was conducted. The subjects were diagnosed as having prediabetes if fasting blood sugar levels ≥100 and <126 mg/dL. The subjects were diagnosed as healthy if fasting blood sugar levels <100 mg/dL. Gutka chewers were defined as individuals who had been chewing ≥1 sachet of gutka daily for ≥1 year and, individuals who reported to have never consumed tobacco in any form were categorized as non-chewers.

In the present study prediabetes with gutka chewers and non-chewers showed no significant difference in periodontal conditions and gingival status. In subjects without prediabetes, gutka chewers had increased PI, BOP and Probing depth compared to non–chewers. Non–chewers in subjects with prediabetes had poorer periodontal conditions compared to gutka chewers and non-chewers in subjects without prediabetes. The results are in agreement to Javed F et al.[19] who investigated the periodontal conditions and oral symptoms among gutka-chewers in subjects with and without type 2 diabetes (T2D), suggesting that subjects without T2D, gutka-chewers have severe periodontal conditions and oral symptoms compared to non-chewers and in subjects with T2D, the severity of these variables is related to glycemic levels rather than gutka consumption.

Thangjam and Kondaiah[31] in their study, demonstrated that the oxidative stress induced by arecoline regulates the inflammatory processes in human keratinocytes. However, the present results suggest that the intensity of oxidative stress induced as a result of hyperglycemia is by far greater than that produced by gutka chewing. It is notable that in this study population, all individuals with prediabetes had raised FBGL compared with those without prediabetes.

In the present study, periodontal parameters like plaque index, sulcus bleeding index and probing depth (4 to <6 mm and ≥6 mm) were higher in prediabetes as compared to healthy patients. Premolar and molar marginal bone loss was higher in the prediabetes group as compared to without prediabetes patients. The results were in accordance with Javed F et al.,[13] demonstrating that self-perceived gingival bleeding and clinical periodontal inflammation were severe in patients with prediabetes as compared with controls.

In the control group (individuals without prediabetes), periodontal inflammatory conditions were worse in gutka chewers compared with non-chewers. One explanation for this difference may be related to the fact that slaked lime (aqueous calcium hydroxide), an essential ingredient in gutka, has been associated with inflammation of the oral mucosa.[32] In parallel, areca nuts contain alkaloids (majorly, arecoline) that jeopardize periodontal tissues.[24] The fact that the non-chewers with prediabetes had more intense periodontal inflammation than gutka chewers without prediabetes may once again be associated with the hyperglycaemic state of the individuals with prediabetes in this study. In this context, prediabetes is the only predictor of periodontal inflammatory conditions in this study population.

In the present study, there was significant differences in PI, BOP, PPD (4 to <6 mm and ≥6 mm) and MBL among gutka chewers and non-chewers in both prediabetes and healthy control group. Prediabetes with and without gutka chewing had significantly higher PI, SBI, PPD (4-6 mm, ≥6 mm) and MBL than healthy non–chewers. These results are correlated to Javed F et al.[33] and the findings suggested that cigarette smokers without prediabetes exhibit significantly severe periodontal disease than non-smokers. In subjects with prediabetes, the severity of periodontal disease seems to be over shadowed by the hyperglycemic state, obscuring the effect of habitual smoking and gutka chewing.

Yen AM et al.[34] in 2006 examined associations between betel-quid chewing and the metabolic syndrome, allowing for recognized risk factors and exploring dose-response effects in a population-based study. Findings concluded that after adjustment for well-established risk factors, study showed independent predictive dose-response effects of betel-quid chewing for the metabolic syndrome and its components in a population-based study of men with a 15% prevalence of betel-nut chewing.

An association exists between bone loss, as observed on panoramic radiographs, and clinical periodontal evaluation.[35] Therefore, panoramic radiographs can be substituted for full-mouth intraoral radiographs.[36] Computer-based measurements for MBL may be advantageous compared to the use of handheld instruments, such as a metric rule or caliper. Additionally, image-processing programs may be used to improve the visual quality of the radiograph, enhance a selected region on the panoramic radiograph, and visualize bone height in different contrasts. Such features of computer-based imaging may assist in the detection of minor bony changes, which may otherwise be overlooked.[37] Hildebolt CF et al.[38] also reported a 40% improvement in results with the use of computer based methods compared to manual measurement. Based on these advantages, we chose computer based programs for measuring the MBL. In the present study, MBL was 2.1 times greater in the premolar and molar regions in prediabetes compared to healthy individuals. MBL was 1.6 times greater in the premolar and molar regions in poorly controlled T2D compared to well-controlled T2D.[38] The present study supported these results.

In the present study the OR of periodontal inflammation in individuals with prediabetes were nine times higher than in healthy control. Gutka chewing alone, chewing among individuals with prediabetes, and chewing among healthy controls did not significantly increase the odds of periodontal inflammatory conditions and concluded that the severity of periodontal inflammation is governed by hyperglycemia when compared to habitual gutka usage. These results are in agreement with Hausmann E et al.[10] where periodontal inflammatory parameters (PI, BOP, and PD) were significantly higher in individuals with prediabetes irrespective of gutka-chewing habit.

Since patients with prediabetes were nine times more susceptible to periodontal inflammation than control individuals (irrespective of the gutka-chewing habit). It seems that the hyperglycemic state in individuals with prediabetes boosts oxidative stress and pro-inflammatory proteins, which in turn masks the contribution of gutka consumption toward jeopardizing periodontal tissues. Multivariate analysis of the predictors of periodontal inflammation also showed pre-diabetic status to be a stronger predictor of periodontal inflammation than gutka chewing habit. However, further studies involving gutka chewers with prediabetes and non-chewers with prediabetes with controlled glycemic status (FBGL ≤100 mg/dL) are warranted to investigate the influence of gutka chewing on periodontal health.

Although most physicians usually depend on blood chemistry values for the diagnosis and management of hyperglycemia, it is highly recommended that patients with prediabetes (particularly those with FBGL >100 mg/dL and with complaints of the onset of gingival bleeding) should also be referred to oral health care providers because these patients are more susceptible to periodontal breakdown compared with patients with prediabetes maintaining FBGL <100 mg/dL.

Overall, the findings reported in this investigation are in agreement with data reported by others.[13],[19],[33] In general, it is already known that parameters of periodontal inflammatory diseases are worse among patients with prediabetes compared with those with healthy individuals. Along these lines, the present study have shown that parameters of periodontal disease (clinical, radiographic, and self-reported, etc.,) are worse in patients with prediabetes.


The present study was an attempt to investigate the severity of periodontal inflammatory conditions in gutka chewers with and without prediabetes. It could be concluded that severity of periodontal inflammation is higher in gutka chewers with prediabetes compared with non-chewers with prediabetes and gutka chewers without prediabetes.

Prediabetes and gutka chewing are significant risk factors for periodontal parameters, and marginal bone loss are independent risk factors for disease severity.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.


1Savage A, Eaton KA, Moles DR, Needleman I. A systematic review of definitions of periodontitis and methods that have been used to identify this disease. J Clin Periodontol 2009;36:458-67.
2Kinane DF, Bartold PM. Clinical relevance of host response and periodontitis. Periodontol 2000 2007;43:278-93.
3Shafique K, Zafar M, Ahmed Z, Khan NA, Mughal MA, Imitaz F. Areca nut chewing and metabolic syndrome: Evidence of a harmful relationship. Nutr J 2013;12:67.
4Pucher J, Stewart J. Periodontal disease and diabetes mellitus. Curr Diab Rep 2004;4:46-50.
5Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease: A summary of current work. Lab Invest 1976;34:235-49.
6Loe H. Periodontal disease. The sixth complication of diabetes mellitus. Diabetes Care 1993;16:329-34.
7Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makrilakis K, et al. Periodontitis and diabetes: A two-way relationship. Diabetologia 2012;55:21-31.
8Javed F, Al-Askar M, Al-Hezaimi K. Cytokine profile in the gingival crevicular fluid of periodontitis patients with and without type 2 diabetes: A literature review. J Periodontol 2012;83:156-61.
9Santos VR, Lima JA, Miranda TS, Feres M, Zimmermann GS, Nogueira-Filho GR, et al. Relationship between glycemic subsets and generalized chronic periodontitis in type 2 diabetic Brazilian subjects. Arch Oral Biol 2012;57:293-9.
10Javed F, Nasstrom K, Benchimol D, Altamash M, Klinge B, Engstrom PE. Comparison of periodontal and socioeconomic status between subjects with type 2 diabetes mellitus and non-diabetic controls. J Periodontol 2007;78:2112-19.
11Demmer RT, Holtfreter B, Desvarieux M, Jacobs DR, Kerner W, Nauck H, et al. The influence of type 1 and type 2 diabetes on periodontal disease progression: Prospective results from the Study of Health in Pomerania (SHIP). Diabetes Care 2012;35:2036-42.
12Javed F, Klingspor L, Sundin U, Altamash M, Klinge B, Engstrom PE. Periodontal conditions, oral Candida albicans and salivary proteins in type 2 diabetic subjects with emphasis on gender. BMC Oral Health 2009;9:12.
13Javed F, Al-Askar M, Al-Rasheed A, Babay N, Galindo-Moreno P, Al-Hezaimi K. Comparison of self-perceived oral health, periodontal inflammatory conditions and socioeconomic status in individuals with and without prediabetes. Am J Med Sci 2012;344:100-4.
14Chang PC, Chien LY, Yeo JF, Wang YP, Chung MC, Chong LY, et al. Progression of periodontal destruction and the roles of advanced glycation end products in experimental diabetes. J Periodontol 2013;84:379-88.
15Manouchehr-Pour M, Spagnuolo PJ, Rodman HM, Bissada NF. Comparison of neutrophil chemotactic response in diabetic patients with mild and severe periodontal disease. J Periodontol 1981;52:410-5.
16Olson DE, Rhee MK, Herrick K, Ziemer DC, Twombly JG, Phillips LS. Screening for diabetes and prediabetes with proposed A1C-based diagnostic criteria. Diabetes Care 2010;33:2184-9.
17American Diabetes Association. Diagnosis and classification of diabetes mellitus (Position Statement). Diabetes Care 2012;35:S64-71.
18The Diabetes Prevention Program (DPP) Research Group. The diabetes prevention program (DPP): Description of lifestyle intervention. Diabetes Care 2002;25:2165-71.
19Javed F, Altamash M, Klinge B, Engstrom PE. Periodontal conditions and oral symptoms in gutka chewers with and without type 2 diabetes. Acta Odontol Scand 2008;66:268-73.
20Javed F, Chotai M, Mehmood A, Almas K. Oral mucosal disorders associated with habitual gutka usage: A review. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;109:857-64.
21Warnakulasuriya S, Trivedy C, Peters TJ. Areca nut use: An independent risk factor for oral cancer. BMJ 2002;324:799-800.
22Bathi RJ, Parveen S, Burde K. The role of gutka chewing in oral submucous fibrosis: A case-control study. Quintessence Int 2009;40:e19-25.
23Javed F, Bello Correra FO, Chotai M, Tappuni AR, Almas K. Systemic conditions associated with areca nut usage: A literature review. Scand J Public Health 2010;38:838-44.
24Jeng JH, Hahn LJ, Lin BR, Hsieh CC, Chan CP, Chang MC. Effects of areca nut, inflorescence piper betle extracts and arecoline on cytotoxicity, total and unscheduled DNA synthesis in cultured gingival keratinocytes. J Oral Pathol Med 1999;28:64-71.
25Yong JC, Hyeon CK, Hee MK, Seok WP, Jongoh K, Dae JK. Prevalence and management of diabetes in Korean adults: Korea National Health and Nutrition Examination Surveys 1998–2005. Diabetes Care 2009;32:2016-20.
26Balkau B, Charles MA. Comment on the provisional report from the WHO consultation. European Group for the Study of Insulin Resistance (EGIR). Diabet Med 1999;16:442-3.
27De Roy PG. Helsinki and the Decleration of Helsinki. World Med J 2004;50/1:9.
28Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J 1975;25:229-35.
29Muhlemann HR, Son S. Gingival sulcus bleeding — A leading symptom in initial gingivitis. Helv Odontol Acta 1971;15:107-13.
30Armitage GC, Svanberg GK, Loe H. Microscopic evaluation of clinical measurements of connective tissue attachment levels. J Clin Periodontol 1977;4:173-90.
31Thangjam GS, Kondaiah P. Regulation of oxidative stress responsive genes by arecoline in human keratinocytes. J Periodontal Res 2009;44:673-82.
32Nair UJ, Friesen M, Richard I, MacLennan R, Thomas S, Bartsch H. Effect of lime composition on the formation of reactive oxygen species from areca nut extract in vitro. Carcinogenesis 1990;11:2145-8.
33Javed 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;345:94-8.
34Yen AM, Chiu YH, Chen LS, Wu HM, Huang CC, Boucher BJ, et al. A population-based study of the association between betel-quid chewing and the metabolic syndrome in men. Am J Clin Nutr 2006;83:1153-60.
35Walsh TF, Al-Hokail OS, Fosam EB. The relationship of bone loss observed on panoramic radiographs with clinical periodontal screening. J Clin Periodontol 1997;24:153-7.
36Persson RE, Tzannetou S, Feloutzis AG, Bragger U, Persson GR, Lang NP. Comparison between panoramic and intra-oral radiographs for the assessment of alveolar bone levels in a periodontal maintenance population. J Clin Periodontol 2003;30:833-9.
37Mol A. Imaging methods in periodontology. Periodontol 2000 2004;34:34-48.
38Hildebolt CF, Brunsden B, Yokoyama-Crothers N, Pilgram TK, Townsend KE, Vannier MW, et al. Comparison of reliability of manual and computer intensive methods for radiodensity measures of alveolar bone loss. Dentomaxillofac Radiol 1998;27:245-50.