Tobacco use as a risk indicator for periodontal disease in a sample of northwestern Ontario residents.

ABSTRACT

Background: The primary objective of the present study was to investigate the relationship between periodontal health, oral hygiene practices, and tobacco use in a cross-sectional study of adults in an urban community in Northwest Ontario. Methods: One hundred individuals between the ages of 19 and 80 participated. The sample consisted of 48% non smokers, 20% current smokers, and 32% former smokers. All participants were given a comprehensive periodontal examination, which included plaque score, calculus score, bleeding on probing, probing depth, and clinical attachment level on all teeth present. A brief medical history and information regarding oral hygiene practices and smoking behaviours were obtained through a questionnaire. Of the participants, 42% had moderate amounts of plaque, with only 26% having a light amount of plaque. Periodontal examinations revealed the following percentages among participants: 28% gingivitis, 36% slight periodontitis, 27% moderate periodontitis, and 9% advanced periodontitis. The average probing depth was 2.42 mm and the average clinical attachment level was 4.37 mm. Results: Advanced periodontal disease among individuals that ever smoked (henceforth referred to as 'ever smokers'), current smokers, and former smokers was twice that of non smokers. Ever smokers were more than twice as likely to present moderate to heavy amounts of calculus and plaque compared to non smokers. Conclusion: The sample showed an observable prevalence of periodontal disease as well as a strong association between cigarette smoking and the risk of periodontal disease among northwestern Ontario residents.

RESUME

Contexte: La presente etude a pour objet principal d'examiner les reports entre I'etat de sante du parodonte, les pratiques d'hygiene buc-cale et le tabagisme dans le cadre d'une recherche transversale menee aupres d'adultes d'une communaute urbaine du nord-est de I'Ontario. Methodes: Cent personnes, dont I'age variait entre 19 et 80 ans, ont participe a I'etude. L'echantillonnage comprenait 48 pour cent de non-fumeurs, 20 pour cent de fumeurs et 32 pour cent d'anciens fumeurs. Les participants ont tous subi un examen parodontal complet, comprenant I'accumulation de la plaque, I'accumulation du tartre, le saignement au sondage, la profondeur de sondage et le niveau d'attache clinique a toutes les dents. Un bref questionnaire a permis de recueillir I'anamnese et 1'information sur less pratiques d'hygiene buccale. Les examens ont donne les resultats suivants: 28 pour cent de gingivites, 36 pour cent de parodontites legeres, 27 pour cent de parodontites moderees et 9 pour cent de parodontites avancees. La profondeur moyenne de sondage etait de 4,37 mm. Resultats: II y a deux fois plus de maladies parodontales avancees chez les gens qui ont toujours fume (*fumeurs inveters*) et les fumeurs actuels et anciens que chez les non-fumeurs. Les anciens fumeurs avaient au moins deux fois plus tendance que les non-fumeurs a developper d'importantes quantites de tartre et de plaque. Conclusion: L'echantillonnage a montre la prevalence des maladies parodontales ainsi qu'une forte association entre le tabagisme et le risque de maladie parodontale chez les residents du nord-ouest de I'Ontario.

Key words: periodontal diseases, smoking, periodontal attachment loss

INTRODUCTION

In addition to the many known cardiovascular and respiratory disease conditions both directly and indirectly associated with smoking and the use of tobacco products, research has also demonstrated that tobacco use is a significant risk factor for the development and progression of periodontal disease. (1-4) Although there is a large variability in association, smokers are 2-14 times more likely to develop periodontal disease than non smokers. (5), (6)

Although general acceptance of a common definition of periodontal disease does not exist, oral health continues to be studied with a variety of demarcation points that differentiate disease from non disease. The definition of the periodontal disease is an important factor that can be expected to contribute to the variation in the magnitude of risk estimates. (7) Typically, oral health is evaluated using clinical and radiographic variables that are useful in providing estimates of prevalence and severity of periodontal disease. (8) Commonly used variables include alveolar bone height, number of missing teeth, oral hygiene, clinical attachment level (CAL), probing pocket depth, gingival recession, tooth mobility, bleeding on probing (BOP), plaque index (PI), and the amount and location of calculus. (8), (9) The effects of smoking on such variables as BOP, amount of plaque and/or calculus, probing depth (PD), clinical attachment loss and gingival recession are inconsistent. For example, while many studies reported comparable plaque levels among smokers versus non smokers, other researchers reported higher plaque levels among smokers. (10-15) Likewise, the specific effects of tobacco smoking on severity of both supra- and sub-gingival calculus have received little research attention except for a single study in which supra- and sub-gingival calculus was reported to be higher. (16)

Although there have been many improvements in oral health behaviours by the general patient population, periodontal disease has remained prevalent and shows little sign of a decline in severity. (17) National clinical epidemiological studies from developed countries have repeatedly estimated that over 90 per cent of the general population has some form of periodontal disease, (18), (19) while between 10%-20% of the population has a severe form of periodontal disease. (20), (21) The prevalence of periodontal disease indicators among adults and the association between tobacco use and periodontal disease in Canadian cohorts is lacking. (22-25)

The primary objective of the present study was to investigate the relationship between periodontal health, oral hygiene practices, and tobacco use in a cross-sectional study of adults in an urban community in Northwest Ontario. A secondary objective was to determine prevalence of periodontal disease within the entire sample, regardless of smoking status.

METHODS

Participants:

The sample consisted of 100 adults recruited from a community college dental clinic, Confederation College Dental Clinic, Thunder Bay, Ontario, Canada. The sample size was based on a 95 per cent confidence interval with 10 per cent error from a reference population of 82,110. (26) An attempt was made to use a randomized approach to select subjects from individuals who visited the clinic; however, the actual subject group represents a convenience sample. Participants were included in the study if they were at least 19 years of age. There were no specific exclusion criteria. All participants received a comprehensive periodontal examination described below. The researcher distributed a questionnaire in the waiting room to collect demographic data as well as information about the patient's medical history, oral health behaviours, and tobacco use using binary, ordinal, and open-ended questions. The socioeconomic status of the sample was not identified to reduce the chance of non-responding. Prior to participation in the study, the participants signed the consent form outlining the study and enabling the researcher to access their dental records. The Lakehead University Research Ethics Board approved this study according to the ethical standards of the Tri-Council Policy Statement for Ethical Conduct for Research Involving Humans 1998.

Periodontal Examination:

The subjects were assessed over a three-month period. All data were collected at a single visit during a regular scheduled dental appointment. Clinical assessments of the patients were conducted by a group of fifteen dental hygiene students. To ensure accuracy, four different trained and experienced dental hygiene clinical instructors (two dentists and two hygienists) remeasured PDs and reevaluated the classification of disease for each patient in an attempt to establish the validity of the initial measures. However, no inter-rater reliability estimates were established between the clinicians, which may be considered a limitation in the generalizability of these estimates. A mouth mirror and Williams probe no. 6 with black markings (Hu-Friedy) were used for all examinations. A Nabers probe (Hu-Friedy) was used to measure furcations. The teeth were dried with compressed air and isolated as necessary.

All teeth present were examined; specifically six sites were examined for PD and BOP. These sites included mesial, mid, and distal of the buccal and lingual aspects. Gingival recession was measured on two sites of each tooth the midbuccal and midlingual sites. All teeth in each of the four quadrants were examined, but third molars were excluded in the analysis. Periodontal examinations included number of teeth, plaque score, sub- and supra-gingival calculus scores using an ordinal scale for calculus as none, light, moderate, or heavy, assigned by visual inspection, gingival status characteristics (colour, consistency, texture, marginal and papillary contours), periodontal case type (based on standard criteria of the 1999 Workshop of Classification of Periodontal Diseases and Conditions), number of teeth mobile, furcation involvement, presence of suppuration, BOP percentage (classified as absent or present for each tooth), PD, and gingival recession.

Plaque was scored using the Silness and Loe Plaque Index for all teeth. Patients were classified as demonstrating light (<:10% covered with plaque), moderate (10%-30%) or heavy (>:30%) plaque scores. The same classification system was used for calculus scoring. The periodontal examination involved the measurement of pocket depths, recorded as the distance from the free gingival margin to the base of the pocket, measured at six sites on all teeth. These sites are the mesial, mid- and distal of the buccal and lingual aspects. Gingival recession was measured on two sites of each tooth; the midbuccal and midlingual sites. Recession was measured as the distance from the cementoenamel junction to the height of the free gingival margin. CAL was calculated as the sum of the gingival recession and PD, BOP, mobility, and furcation involvement was not given a grade; instead, each variable was calculated as a dichotomous variable. The number of BOP sites was recorded and tabulated as a percentage ([number of bleeding sites[bi] number of sites probed] x 100). Severe periodontal disease was classified as having a mean clinical attachment loss >4.5 mm consistent with the recommendations of the 1999 Workshop of Classification of Periodontal Disease and Conditions. (27)

Smoking Status Assessment:

Smoking status was assessed by a self reported questionnaire. Participants were asked to estimate the number of cigarettes consumed per day and the number of years they smoked. Current smokers were individuals who were smoking at the time of the examination. Former smokers were individuals who had quit smoking at the time of the examination. Former smokers were also asked to report time since quitting, as well as number of years using tobacco and frequency of use; however, the researchers did not confirm the participants' responses using external validation. The type of tobacco product used for example, cigarette, pipe, or cigar was recorded. Smoking exposure was expressed in terms of "pack year", which is the division of the number of cigarettes smoked per day by the multiplication of the number of cigarettes in a pack, the number of days in a year, and the number of years smoked.

Data Processing and Statistical Analysis:

Three electronic databases were created for data entry. Clinical variables including, number of teeth, average PD, and average CAL were computed for each subject and averaged for the groups of tobacco users versus non users. Descriptive statistics, which included means, variances, and frequencies, were computed for oral hygiene and smoking behaviours measured via the patient questionnaire. Frequency distributions were used to evaluate amount of plaque, case type, and characteristic variables, which describe gingival characteristics. Comparisons between continuous variables were analyzed using ANOVA (alpha = 0.05), while chi-square goodness of fit analyses were used to evaluate categorical data. Linear regression was used to measure significance when evaluating the accuracy of the assessment performed by the clinical team. For many of the analyses, both current and former smokers were grouped together and termed ever smokers to enable a sufficient number of subjects within each analysis subgroup.

Table 1: Characteristics of study sample (n = 100)

Characteristic                                        %

Gender

  Male                                              48
  Female                                            52

Age (years)

  [less than or equal to] 40 (range 19-40)          60
  41-60                                             22
  >60 (range 61-80)                                 18
Under the care of a physician                       23
Currently taking a medication                       43
Smoking Status
  Current smokers                                   20
  Former smokers                                    32
  Non smokers                                       48

Visits to dentist

  Regularly                                         50
  Not regularly                                     50

Frequency of professional dental cleaning (months)

  >3<6                                               4
  6-12                                              40
  12-24                                             34
  >24                                               19
  Never                                              3

Frequency of brushing

  More than 1 x/day                                 73
  1 x/day                                           22
  <1/day                                             5
  >1/week                                            0
  Never                                              0
Frequency of flossing
  More than 1 x/day                                  8
  1 x/day                                           34
  <1x/day                                           21
  <1 x/week                                         27
  Never                                             10

Bleeding of gingiva when brush/floss

  Bleeding                                          41
  No bleeding                                       59

Case type

  Gingivitis (Case I)                               28
  Slight Periodontitis (Case II)                    36
  Moderate Periodontitis (Case III)                 27
  Advanced Periodontitis (Case IV)                   9
  Refractory (Case V)                                0
Plaque
  Light                                             26
  Moderate                                          42
  Heavy                                             32

RESULTS

All participants completed both the questionnaire and the periodontal examination. Demographic characteristics, self reported oral hygiene practices, and periodontal status of the subjects are shown in Table 1. The average age ([+ or -] standard deviation) of the sample was 40 [+ or -] 17 years.

Chi-square goodness of fit analysis ([rho]> 0.05) showed that there was no association between mean clinical attachment loss and the use of prescribed medications; or between mean clinical attachment loss and the presence of one or more medical conditions.

Prevalence of tobacco use:

Although nearly 80 per cent of the participants in this study self classified as non smokers, categorizing the smokers by gender showed an equal proportion of current and former smokers among males; however, there were more former smokers among females (n = 6 current smokers). Smokers were on average younger than non smokers [average age age smokers [+ or -] standard deviation (SD) = 36.6 [+ or -] 15.1, average age non smokers [+ or -] SD= 43.7 [+ or -] 18.77]. The majority of former tobacco users indicated they smoked cigarettes, with one individual indicating he/she used both smoke less tobacco and smoked cigarettes; only one participant reported using a pipe for tobacco smoking.

Oral hygiene of the sample:

Almost 60 per cent of the sample reported having a standard dental hygiene visit every 6-24 months. Ninety-five per cent of the sample reported that they brushed at least daily, with only 42 per cent flossing daily. An inconsistency between the reported practices and the evaluated plaque scores was apparent; 74 per cent of the sample had moderate or heavy amounts of plaque.

Periodontal status of sample:

It is important to note that all participants had, at a minimum, a mean value of > 2.5 mm clinical attachment loss. Age did not predict PD or CAL. When categorized by case type based on the standard criteria of the 1999 Workshop of Classification of Periodontal Disease and Conditions, the percentage of individuals were equal between case type I (gingivitis), II (slight periodontitis), and III (moderate periodontitis), with slightly more participants presenting with slight periodontitis.

Tobacco consumption:

Questions about tobacco use comprised the majority of the questionnaire. Table 2 illustrates the variables examined with regard to tobacco use and gender. Chi square goodness of fit analysis showed no significant difference between CAL and either amount or duration of smoking, or between PD and "pack years" within the cohort of current smokers (n = 20). Former and current male tobacco users were users longer and reported higher volumes of tobacco per day compared to females. Former smokers reported using higher volumes of tobacco than current smokers. The age of initiation in both the male and female cohorts was, on average, 16 years.

Table 2: Tobacco use variables by gender (Mean [+ or -] SD)
Variable                 Former smoker

                          Male (n=14)          Female (n=18)

Average years          12.5 [+ or -] 14.1   10.3 [+ or -] 9.95
since quit

Duration (years)        9.14 [+ or -] 7.4     5.8 [+ or -] 5.5

No. of cigarettes/day  13.8 [+ or -] 11.0     9.7 [+ or -] 8.3

Age of initiation               -                    -
(years)

No. of last 30 days             -                    -
smoked (days)

Variable                         current smoker

                          Male (n=11)       Female (n=6)

Average years                  -                   -
since quit

Duration (years)       14.9 [+ or -] 12.3  11.0 [+ or -] 2.4

No. of cigarettes/day   12.0 [+ or -] 8.2   9.3 [+ or -] 3.2

Age of initiation       15.9 [+ or -] 4.1  16.3 [+ or -] 3.7
(years)

No. of last 30 days     27.5 [+ or -] 7.5  28.5 [+ or -] 3.2
smoked (days)

Of the current cigar users (n = 7), the average number of cigars smoked per day was 1.3 [+ or -] 0.75 over an average of 5.7 [+ or -] 4.2 years. One current chewing tobacco user indicated that he/she used chewing tobacco every day for the past 10 years, and one participant reported occasionally smoking 1 pipe per day for the past 10 years.

Smoking status and periodontal status:

As shown in Table 3, periodontal related variables were assessed in relationship to smoking status. Current smokers had deeper mean PDs, compared to former and non smokers. Former smokers had greater mean clinical attachment loss than both current and non smokers. Clinical attachment loss was grouped into 4 categories as follows, [less then or equal to] 3.5 mm, > 3.5 [less then or equal to] 4.5mm, > 4.5 [less then or equal to] 5.5 mm, and > 5.5 mm. The results of the goodness of fit test applied to the association between CAL and smoking status was not significant ([rho] < 0.066), however, the difference should be further investigated as a higher prevalence of clinical attachment loss was observed among the ever smokers compared to the non smokers.

Table 3: Periodontal variables according to smoking status
(Mean [+ or -] SD)

Variable                 Current smokers        Former smoders

Mean PD (mm)           2.44 [+ or -] 0.45    2.45 [+ or -] 0.37
Mean CAL (mm)[dagger]  4.38 [+ or -] 0.82    4.48 [+ or -] 0.78

                           Smoders (currentr + former)

No. of teeth                   26.71 [+ or -] 2.8
B.O.P (%)                      11.06 [+ or -] 9.5

Case type (%)

  Case I                             15 (28%)
  Case II                            16 (30%)
  Case III+1V                        21 (42%)

Supra-gingival calculus
amounts [double dagger]

  None-light                         31 (60%)
  Moderate- Heavy                    21 (40%)


Plaque *

  Light                               9 (17%)
  Moderate-Heavy                     43 (83%)

Variable                    Non smokers          Entire sample

Mean PD (mm)             2.41 [+ or -]0.40     2.42 [+ or -] 0.42
Mean CAL (mm)[dagger]    4.28 [+ or -] 0.91   4.367 [+ or -] 0.085

Variable                    Non smokers          Entire sample

No. of teeth             26.35 [+ or -] 4.15    26.5 [+ or -] 3.5
B.O.P (%)                 9.32 [+ or -]12.0            -

Case type (%)

  Case I                       13 (27%)               28
  Case II                      20 (42%)               36
  Case III+1V                  15 (31%)               36

Supra-gingival calculus
amounts [double dagger]

  None-light                   37 (77%)                -
  Moderate-Heavy               11 (23%)                -

Plaque *

  Light                        17 (35%)               26
  Moderate-Heavy               31 (65%)               74

[dagger] Important difference between smokers (current and former)
and non smokers when categorized using chi-square analysis
(p<0.066, df = 3)
[double dagger] Important difference between groups using
chi-square analysis (p = 0.06)
* Significant difference between groups using chi-square
analysis (p<0.05; df = 1)

The proportion of subjects with gingivitis, slight periodontitis, or moderate to severe periodontitis was assessed. The results showed that moderate to severe periodontitis was more frequent in the cohort of ever smokers.

Odds ratios were used to determine the degree of association between smoking status and CAL, plaque score, and calculus amount (supra- and sub-gingival). The computation showed that the odds of developing severe periodontal disease (CAL > 4.5 mm) were twice as likely (2.08) for ever smokers versus non smokers. The results also showed that ever smokers were 2.62 and 2.38 times more likely to demonstrate moderate to heavy amounts of plaque and calculus, respectively, compared to those who did not smoke. A significant difference was found when comparing smoking status and supra-gingival calculus amounts and plaque scores.

Linear regression between CAL and periodontal case type was used to validate the estimation of the clinical team. The statistically significant association ([rho] < 0.0001) confirmed that the clinical team was accurate and reliable in their CAL assessment and categorizing each patient appropriately.

DISCUSSION

The results of this study support previous research demonstrating that smokers are at greater risk of developing severe periodontal disease than non smokers. (2), (9-11) In this study, we evaluated various aspects of periodontal status. Severe periodontal disease was classified as having a mean CAL of > 4.5 mm. The overall periodontal status included PD and CAL among other assessments. Consistent with other research, the present study found that individuals were twice as likely to develop severe periodontal disease if they smoked. Generally, assessment of risk in other studies showed that smoking was associated with a 2- to 7-fold increase and even up to 11.8-fold increase in risk for having periodontal tissue loss. (2), (6), (9), (11), (23), (28), (29) The large variability in this risk estimate differs across study type and most importantly, the different case definitions of periodontal disease. A narrower definition of periodontal disease could result in higher risk estimates. (23)

When examining the group by smoking status, the non smokers had the lowest average CAL score; whereas former smokers had a higher average CAL than current smokers. This suggests that smoking may have an effect on CAL that appears after prolonged exposure to tobacco and may not be reestablished despite removing exposure. However, the trend in periodontal PDs (which is a determinant of CAL) showed that former smokers had deeper PDs than non smokers but not deeper than current smokers. Therefore, while overall CAL may not recover from smoking cessation, PD may improve from smoking cessation. This study did not focus on how long after cessation oral health benefits can be observed; however, the benefits of cessation outweigh the harmful effects of smoking on periodontal health.

Reported oral hygiene behaviours, specifically, the frequency of visiting a dental professional for dental hygiene maintenance and the frequency of brushing more than once a day was higher than that which was reported by Al-Shammari et al., (30) but more consistent with the behaviours reported by Payne and Locker. (31) Based on the self reported responses, one might be led to believe that this cohort had good oral hygiene behaviours, and were therefore minimally at risk with regard to their access or awareness of dental care. However, as with most dental patients, it should be noted that the technique of brushing and flossing may be mechanically incorrect and more important, that the frequency of preventive dental behaviours was over reported among participants in this sample. The results of PD and clinical attachment measurements support the notion that while participants measurements support the notion that while participants believed that their behaviours were adequate and appropriate, the specific measures demonstrate that these individuals were all at risk for periodontal disease.

The study also showed that self reported oral hygiene behaviours were not considerably different between ever smokers and non smokers. While this finding is important alone, the odds ratios demonstrated that ever smokers were more than twice as likely to show higher levels of plaque as well as both supra- and sub-gingival calculus, noted precursors of gingival inflammation leading to periodontal disease. Despite the best intentions of smokers to maintain good oral health through subscribing to regular dental visits and practices, periodontal disease and its related sequelae continue to develop. The results of the present study which demonstrate higher levels of plaque and calculus among smokers cannot be easily discerned, but may be either the consequence of tobacco exposure or could be attributed to poor brushing and flossing techniques.

Consistent with the Van der Weijden et al. study, (32) no differences in bleeding tendency were detected between ever smokers and non smokers. However, Dietrich (33) reported smokers having less bleeding on probing than non smokers, which has been explained by the vasoconstrictive effects of nicotine on peripheral blood vessels. Conversely, one study, consisting of a cohort of individuals ages 19 to 40, reported smokers having more bleeding. (28)

In the present study, the average CAL of slightly more than 4 mm suggests a higher than expected score, especially in a sample of individuals visiting an urban community dental clinic. Moreover, the reported clinical attachment score suggests that more individuals were experiencing severe periodontal disease than previously reported in other studies. For example, two relevant Canadian research studies (22), (23) reported 2.95 mm and 3.89 mm CALs respectively, when considering the entire sample. As well, another study of similar age distribution reported lower average CALs. (34)

Although half of the participants reported ever using a tobacco product, even fewer indicated that they were current smokers. The prevalence of smokers within the present study (20 per cent) is consistent with the provincial estimate of 20.9 per cent and slightly below the regional estimate of 26.6 per cent. (35)

Although the study demonstrated the residual effects of smoking on periodontal disease, the relatively small number of current smokers may have had a direct influence on several comparisons. In bivariate analyses, several variables were associated with clinical attachment loss. However, some variables were not significant under the ANOVA and/ or Chi-Square tests. For example, a dose-response relationship was not found when "pack years" and mean PDs were compared. The interpretation of this finding, along with others, needs to be treated with caution, as the absence of a significant association may reflect the fact that the number of individuals who reported to be current smokers was too small for a relationship to be assessed.

Socio-economic status has also been reported to be related to smoking habits. (11) Since the socio-economic status of the sample was not identified, these factors may have exerted a confounding influence on the outcome variables implicitly and thus influenced the results.

The specific limitations of this study were related to issues of design, sample size, and reliability of self reported data. The cross sectional design may be considered a limitation because it collected data at a single episode in time, and yet using CAL as a main outcome variable, the researchers were able to demonstrate cumulative periodontal destruction over time. (36) The reliability of self reported data is also a limitation of the study. A measure of external validity was not used in the study to confirm the actual exposures to nicotine or tobacco related products. Thus, the reports of nicotine exposure may be suspect for some individuals who may have been less accurate in their estimates of tobacco product exposure.

The term consumption referred to tobacco product use at the time of the study and did not take into account changes over time or possible intervals when the individual was not smoking. The sample size of 100 respondents was reasonable, although the number of participants that reported tobacco use was consistent with the provincial estimates of smokers in a selected community.

CONCLUSION

This study was intended to be a survey of periodontal health exploring the association between smoking behaviours and periodontal health outcomes in a sample of individuals from Northwest Ontario. To date, few Canadian studies have been published on this topic, and no studies have been reported at the local level pertaining to the effects of tobacco on the periodontium. The current study is useful in that the findings reported here support the suggestion that a relationship exists between smoking and poor periodontal health. Yet most important, these findings suggest that the periodontal health outcomes demonstrated by smokers are observed even after quitting, and may not be reestablished simply by improving oral hygiene practices.

The clinical measurements complemented the information collected from the questionnaire to form a clinical data set in Northwest Ontario that did not previously exist. The research methods used in the present study may be used to initiate ongoing data collection of adults within the area. It is anticipated that this study may be of assistance to dental professionals, researchers and epidemiologists in learning more about the tobacco-periodontal association as well as contributing to the current surveillance of the oral health profile of individuals in the area. This study confirms the need to identify tobacco users within the dental patient cohort. Thus, introducing counselling as a tobacco cessation intervention to prevent periodontal disease should include proper oral hygiene behaviours.

ACKNOWLEDGMENT

This research was supported by an Ashley Studentship for Research in Tobacco Control from the Ontario Tobacco Research Unit.

REFERENCES

(1.) Albandar JM. Global risk factors and risk indicators for periodontal diseases. Periodontol 2000. 2002;29:177-206.

Bergstrom J, Preber H. Tobacco use as a risk factor. J Periodontol. 1994;65:545-550.

(3.) Ogawa H, Yoshihara A, Hirotomi T, Ando Y, Miyazaki H. Risk factors for periodontal disease progression among elderly people. J Clin Perodontol. 2002;29:592-597.

(4.) Rivera-Hidalgo F. Smoking and periodontal disease. Periodontol 2000-2003;32:50-58.

(5.) Grossi SG, Genco RJ, Machtei EE. Assessment of risk for periodontal disease: Risk Indicators for alveolar bone loss. J Periodontol. 1995;66:23-29.

(6.) Papapanou P. Periodontal diseases: Epidemiology. Ann Periodontal. 1996;1:1-36.

(7.) Bergstrom J. Tobacco smoking and risk for periodontal disease. J Clin Periodontol. 2003;30:107-113.

(8.) Lagervall M, Jansson L, Bergstrom J. Systemic disorders in patients with periodontal disease. J Clin Periodontol. 2003;30:293-299.

(9.) Calsina G, Ramon, JM, Echeverria, J-J. Effects of smoking on periodontal tissues. J Clin Periodontol. 2002;29:771-776.

(10.) Bergstrom J, Eliasson S, Dock J. Exposure to tobacco smoking and periodontal health. J Clin Periodontal. 2000;27:61-68.

(11.) Muller HP, Stadermann S, Heinecke A. Gingival recession in smokers and non-smokers with minimal periodontal disease. J Clin Periodontol. 2002;29:129-136.

(12.) Bergstrom J. Oral hygiene compliance and gingivitis expression in cigarette smokers. Scand J Dent Res. 1990;98:497-503.

(13.) Haffajee AD, Socransky SS. Relationship of cigarette smoking to attachment level profiles. J Clin Periodontol. 2001;28:283-295.

(14.) Axelsson P, Paulander J, Lindhe J. Relationship between smoking and dental status in 35-, 50-, 65- and 75- year-old individuals. J Clin Periodontol. 1998;25:297-305.

(15.) Linden GJ, Mullally BH. Cigarette smoking and periodontal destruction in young adults. J Periodontol. 1994;65:718-723.

(16.) Bergstrom J. Tobacco smoking and supragingival dental calculus. J Clin Periodontol. 1999;26:541-547.

(17.) Downer, M.C. The changing pattern of dental disease over 50 years. Br Dent J. 1998;185:36-41.

(18.) Borrell LN, Burt A, Gillespie BW, Lynch J, Neighbors H. Periodontitis in the United States: beyond black and white. J Public Health Dent. 2002;62:92-101.

(19.) Morris AJ, Steele J, White DA. The oral cleanliness and periodontal health of UK adults in 1998. Br Dent J. 2002;91(4):186-92.

(20.) Albandar J, Brunelle J, Kingman A. Destructive periodontal disease in adults 30 years of age and older in the United States, 1988-1994. J Periodontol. 1999;70:13-29.

(21.) Hugoson A, Laurell L. A prospective longitudinal study on periodontal bone height changes in a Swedish population. J Clin Periodontol. 2000;27:665-674.

(22.) Brodeur JM, Payette M, Benigeri M, Charbonneau A, Olivier M, Chabot D. Periodontal diseases among Quebec Adults Aged 35 to 44 years J Can Dent Assoc. 2001;67:34-41.

(23.) Locker D, Leake JL. Risk Indicators and Risk Markers for Periodontal Disease Experience in Older Adults Living Independently In Ontario, Canada. J Dent Res. 1993;72(1):9-17.

(24.) Hoover JN, Tynan JJ. Periodontal status of a group of Canadian adults. J Can Dent Assoc. 1986;52(9):761-763.

(25.) Sbaraglia M, Turnbull R, Locker D. Risk indicators for peiodontal disease in a remote Canadian community- a dental practice-based study. J Public Health Dent. 2002;62(1):51-56.

(26.) Statistics Canada. 2001 Community Profiles. Released June 27, 2002. Last modified: 2005-11-30. Statistics Canada Catalogue no. 93F0053XIE.

(27.) 1999 Workshop for a Classification of Periodontal Diseases and Conditions Ann Periodontal. 1999;4:1-112.

(28.) Haber J, Wattles J, Crowley M, Mandell R, Joshipura K, Kent R L. Evidence for cigarette smoking as a major risk factor for periodontitis. J. Periodontol. 1993;64:16-23.

(29.) Torrungruang K, Nisapakultorn K, Sutdhibhisal S, Tamsai-lom S, Rojanasomsith K, Vanichjakvong O et al. The effect of cigarette smoking on the severity of periodontal disease among older Thai adults. J Periodontol. 2005;76(4):566-572.

(30.) Al-Shammari KF, Al-AnsariJM, Al-Khabbaz AK, Dashti A, Hon-kala EJ. Self-Reported Oral Hygiene Habits and Oral Health Problems of Kuwaiti Adults. Med Princt. 2007;16:15-21.

(31.) Payne BJ, Locker D. Relationship Between Dental and General Health Behaviors in a Canadian Population. J Public Health Dent. 1996;56(4):198-204.

(32.) Van der Weijden GA., De Slegte C, Timmerman MF, Van der Velden U. Periodontitis in smokers and non smokers: intraoral distribution of pockets: A retrospective study. J Clin Periodontol.2001;28:955-960.

(33.) Dietrich T, Bernimoulin JP, Glynn RJ. The effect of cigarette smoking on gingival bleeding. J Periodontol. 2004;71(1):16-22.

(34.) Bagramian R, Farghaly MM, Lopatin D, Sowers MF, Syed SA, Pomerville JL. A comparison of periodontal disease among rural Amish and non-Amish adults. J Clin Periodontol. 199;21:386-390.

(35.) Statistics Canada. Canadian Community Health Survey Cycle 3.1 (2005) http://www.statcan.ca/bsolc/english/bsolc?catno=82-621-X&CHROPG=l

(36.) Loe H, Anerud A, Boysen H, Smith M. The natural history of periodontal disease in man. The rate of periodontal destruction before 40 years of age. J Periodontol. 1978;49:607-620.

Ann Marie Chlebovec, HBSc, MPH, William J. Montelpare, PhD, Bruce R. Pynn, MSc, DDS, FRCD(C)

Lakehead University. Thunder Bay, Ontario

Submitted 25 Sept.2007; Revised 10 Jan.2008; Accepted 24 Jan.2008

This is a peer-reviewed paper.

Correspondence to: William J. Montelpare, Ph.D., School of Kinesiology,

Lakehead University, Thunder Bay, Ontario P7B 5E1

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