242
Cigarette Smoking and
Periodontal
Bone Loss Jan
Bergström, * Sörén Eliasson,f and Hans Preber*
and loss of periodontal bone height was investiThe Swedish dental in hygienists. study group included 210 subjects: 24 to 60 gated 32% former 30% of smokers, and 38% non-smokers. The study was smokers, years age, based on bite-wing radiographs, where loss of the interproximal bone height was measured as the distance from the cemento-enamel junction (CEJ) to the interdental septum (IS). The magnitude of the CEJ-IS distance was read at 12 sites, representing 3 maxillary and 3 mandibular bone septa in each subject. The CEJ-IS distance was significantly greater for smokers when compared to non-smokers, mean ± SEM 1.71 ± 0.08 mm and 1.45 ± 0.04 mm, respectively. The mean ± SEM for former smokers was 1.55 ± 0.05 mm. In smokers, the CEJ-IS distance increased with increased smoking exposure. The results, based on adults with good oral hygiene, suggest that loss of periodontal bone is related to smoking. The smoking related bone loss is not correlated with plaque infection. / Periodontol 1991; 62:242-246. The
association between smoking
Key Words: Smoking/adverse effects; bone loss/etiology; periodontal diseases/etiology. The adverse effects of tobacco smoking on health are well known. The negative effects seem to involve periodontal health. Several investigations indicate a relationship between smoking and periodontal disease, including loss of the alveolar bone.1-9 There is evidence that smoking affects the mineral content of bone tissue. Progressive loss of bone mineral with advancing age is even more prominent in smokers.10"14 It is a matter of argument whether the influence of smoking on the periodontal tissues is a direct one or mediated by plaque infection. Studies in subjects with a high standard of oral hygiene have shown a greater bone loss in smokers than non-smokers.15"16 This suggests a direct influence of smoking on periodontal health irrespective of plaque infection. In order to further elucidate the hypothesis of a direct influence of smoking on periodontal health, an investigation was carried out using dental hygienists. It was expected that dental hygienists were subjects with a very high standard of oral hygiene. Therefore, the confounding influence of plaque infection could be controlled. The main object of the investigation was to study the influence of smoking on the interproximal periodontal bone height by comparing current smokers and non-smokers. Furthermore, former smokers were investigated to see if they held an intermediate position in this respect.
invited to take part in the study. The hygienists were asked to respond to a mailed questionnaire about their smoking habits, their attitudes towards smoking, and their knowledge about smoking-associated health hazards. Moreover, they were asked to enclose a bite-wing radiograph of themselves taken within the last 3 years, and to return it together with the questionnaire. They were informed that the x-ray material would be subjected to bone height evaluation. Out of 325 persons invited 265 (82%) responded to the questionnaire and 210 (65%) enclosed a bite-wing radiograph. Among the respondents contributing a radiograph, 30% were smokers, 32% former smokers, and 38% were non-smokers; i.e. persons with no smoking history (neversmoked). Those individuals currently smoking one or more cigarettes a day were considered smokers. Individuals who had previously been regularly smoking but stopped more than 1 year ago were labeled former smokers. The relative frequencies of smokers, former smokers, and non-smokers among respondents contributing a radiograph coincided closely to that of the total sample of respondents. Furthermore, the relative frequencies among non-radiographic
MATERIAL AND METHODS All dental hygienists living in Stockholm county and affiliated with the Swedish Dental Hygienist Association in 1987
was 38.4 years and there were differences with respect to age statistically significant between the smoking groups. The mean age among questionnaire-only respondents was 37.5 years with no significant differences between smoking groups.
'Department of Periodontology, Karolinska Institutet, Stockholm, department of Oral Radiology.
Sweden,
were
were quite similar, 31% smokers, 34% former smokers, and 35% non-smokers. The present study group by age and smoking is presented
questionnaire-only respondents in Table 1. The no
mean
age
Volume 62 Number 4 Table 1:
BERGSTRÖM, ELIASSON, PREBER Table 5: Number of Site-Specific Measurements of Bone Height Included in Case Mean (Mean and SEM for smokers and non-
Study Group According to Age and Smoking Age
Current smokers Former smokers Non-smokers *Number of
63 67
smokers)
Mean
SD
Range
37.4 39.9 37.5
7.33 7.99 9.04
25-56 25-56 24-60
of Smokers
Frequency Distribution Consumption 15
_(%)
_(%)
(16) (31) (24)
10 21 31
Years of
20
19
21
63 67 130
Smoking
16-20
(%) (30)
(%) (33)
Total
(6) (14) (10)
4 9 13
Table 3: Frequency Distribution of Smokers Duration
16.5
25.4
of Smokers
According to Lifetime
Exposure (cigarette/years) 200
_(%) ti_(%) Current smokers Former smokers Total Mean exposure
Total
63
(%) (100)
Mean exposure 158
25
(40)
25
(40)
13
(%) (20)
38
(57)
16
(24)
13
(19)
67
(100)
127
63
(48)
41
(32)
26
(20)
130
(100)
137
52
127
291 -
-
The frequency distributions of current smokers and forsmokers by cigarette consumption and smoking duration appear in Tables 2 and 3, respectively. Mean consumption was 9.9 and 11.2 cigarettes/day among current smokers and former smokers, respectively, and mean duration was 16.5 years and 10.8 years, respectively. The lifetime smoking exposure as derived from the product of the number of years of smoking and stated cigarette consumption (cigarette-years)17 for current smokers and former smokers is presented in Table 4. Comparison of bone height in different smoking exposure groups was performed after adjustment for differences in age using bone height in nonsmokers as reference. mer
(n 63) =
Sites
Maxillary
Mean 4.8 4.8 9.5
Non-smokers
Total
(n 80)
(n 143)
=
SEM
Mean
0.17 0.19 0.31
5.1 5.2 10.2
SEM 0.14 0.12 0.23
=
Mean 5.0
4.9 9.9
SEM 0.08 0.08 0.15
According to Cigarette
Consumption per Day Current smokers Former smokers Total
Smokers
Mandibular All
subjects.
Table 2:
243
The bite-wing radiograph represented the molar and premolar areas of the right side of the dentition. The distance from the cemento-enamel junction (CEJ) to the interdental septum (IS) was measured mesially and distally for all teeth from 14 to 17 and from 44 to 47. The mesial measurement of first premolare and the distal one of second molars were omitted. Thus a maximum of 12 sites representing 3 maxillary and 3 mandibular periodontal bone septa were available for measurement in each subject. The radiographs were read by one observer under a 7 x magnification and measurements were made to the nearest 0.1 mm. The observer performing the measurements was unaware of the smoking status of the individual subjects. The method and its precision of bone height measurements have been presented elsewhere.18 The measurability for the different predetermined sites varied from 71% to 88% with no systematic differences between smoking groups. The number of measurements included in the means of the subjects ("case-means") forming the maxillary, mandibular, and overall CEJ-IS values are presented in Table 5. Altogether, in 95% of subjects the overall case-mean was based on 6 or more site specific measurements. The presence of radiographically detectable calculus was examined on the same bite-wing radiographs for each proximal tooth surface corresponding to the interdental crest regions analyzed for bone height. Thus a maximum of 12 dental surfaces were examined in the subject. The habitual oral hygiene standard was evaluated in 19 individuals, selected at random, 8 smokers and 11 nonsmokers. The mean ± SEM age was 33.6 ± 2.15 years (range 25 to 42 years) in smokers and 36.7 ± 2.25 years (range 28 to 52 years) in non-smokers. Mean ± SD consumption among smokers was 15.0 ± 5.9 cigarettes/day. The plaque index was measured according to the method of Silness and Löe19 by one observer, unaware of the smoking status. The mean ( ± SEM) plaque index was 0.28 ± 0.03 and 0.33 ± 0.04 for smokers and non-smokers, respectively. The difference between the means was not sta-
tistically significant (/
=
1.07,
>
0.05).
Statistics Statistical significance of differences between means was tested by the Student r-distribution, two-tailed, or, if the variances differed, by Pitman's permutation test. Multiple regression analysis was carried out with the CEJ-IS distance as de-
244
J Periodontol April 1991
SMOKING AND BONE LOSS
MANDIBULAR SITES
CEJ-1S DISTANCE
(mm)
3.0
SMOKER EX-SMOKER
2.0
NON-SMOKER NON-SMOKER
1.0
Site 47/46
Site 46/45
Site 45/44
A MANDIBULAR SITES
regression of
Table 6: The CEJ-IS Distance and Cigarette Consumption
SMOKER EX-SMOKER
(mm)
10 Mean
10 Mean
SEM
1.51 2.71 2.06
0.157 0.407 0.205
Pitman's test >0.05
Cigarette Smoking and
Periodontal
Bone Loss Jan
Bergström, * Sörén Eliasson,f and Hans Preber*
and loss of periodontal bone height was investiThe Swedish dental in hygienists. study group included 210 subjects: 24 to 60 gated 32% former 30% of smokers, and 38% non-smokers. The study was smokers, years age, based on bite-wing radiographs, where loss of the interproximal bone height was measured as the distance from the cemento-enamel junction (CEJ) to the interdental septum (IS). The magnitude of the CEJ-IS distance was read at 12 sites, representing 3 maxillary and 3 mandibular bone septa in each subject. The CEJ-IS distance was significantly greater for smokers when compared to non-smokers, mean ± SEM 1.71 ± 0.08 mm and 1.45 ± 0.04 mm, respectively. The mean ± SEM for former smokers was 1.55 ± 0.05 mm. In smokers, the CEJ-IS distance increased with increased smoking exposure. The results, based on adults with good oral hygiene, suggest that loss of periodontal bone is related to smoking. The smoking related bone loss is not correlated with plaque infection. / Periodontol 1991; 62:242-246. The
association between smoking
Key Words: Smoking/adverse effects; bone loss/etiology; periodontal diseases/etiology. The adverse effects of tobacco smoking on health are well known. The negative effects seem to involve periodontal health. Several investigations indicate a relationship between smoking and periodontal disease, including loss of the alveolar bone.1-9 There is evidence that smoking affects the mineral content of bone tissue. Progressive loss of bone mineral with advancing age is even more prominent in smokers.10"14 It is a matter of argument whether the influence of smoking on the periodontal tissues is a direct one or mediated by plaque infection. Studies in subjects with a high standard of oral hygiene have shown a greater bone loss in smokers than non-smokers.15"16 This suggests a direct influence of smoking on periodontal health irrespective of plaque infection. In order to further elucidate the hypothesis of a direct influence of smoking on periodontal health, an investigation was carried out using dental hygienists. It was expected that dental hygienists were subjects with a very high standard of oral hygiene. Therefore, the confounding influence of plaque infection could be controlled. The main object of the investigation was to study the influence of smoking on the interproximal periodontal bone height by comparing current smokers and non-smokers. Furthermore, former smokers were investigated to see if they held an intermediate position in this respect.
invited to take part in the study. The hygienists were asked to respond to a mailed questionnaire about their smoking habits, their attitudes towards smoking, and their knowledge about smoking-associated health hazards. Moreover, they were asked to enclose a bite-wing radiograph of themselves taken within the last 3 years, and to return it together with the questionnaire. They were informed that the x-ray material would be subjected to bone height evaluation. Out of 325 persons invited 265 (82%) responded to the questionnaire and 210 (65%) enclosed a bite-wing radiograph. Among the respondents contributing a radiograph, 30% were smokers, 32% former smokers, and 38% were non-smokers; i.e. persons with no smoking history (neversmoked). Those individuals currently smoking one or more cigarettes a day were considered smokers. Individuals who had previously been regularly smoking but stopped more than 1 year ago were labeled former smokers. The relative frequencies of smokers, former smokers, and non-smokers among respondents contributing a radiograph coincided closely to that of the total sample of respondents. Furthermore, the relative frequencies among non-radiographic
MATERIAL AND METHODS All dental hygienists living in Stockholm county and affiliated with the Swedish Dental Hygienist Association in 1987
was 38.4 years and there were differences with respect to age statistically significant between the smoking groups. The mean age among questionnaire-only respondents was 37.5 years with no significant differences between smoking groups.
'Department of Periodontology, Karolinska Institutet, Stockholm, department of Oral Radiology.
Sweden,
were
were quite similar, 31% smokers, 34% former smokers, and 35% non-smokers. The present study group by age and smoking is presented
questionnaire-only respondents in Table 1. The no
mean
age
Volume 62 Number 4 Table 1:
BERGSTRÖM, ELIASSON, PREBER Table 5: Number of Site-Specific Measurements of Bone Height Included in Case Mean (Mean and SEM for smokers and non-
Study Group According to Age and Smoking Age
Current smokers Former smokers Non-smokers *Number of
63 67
smokers)
Mean
SD
Range
37.4 39.9 37.5
7.33 7.99 9.04
25-56 25-56 24-60
of Smokers
Frequency Distribution Consumption 15
_(%)
_(%)
(16) (31) (24)
10 21 31
Years of
20
19
21
63 67 130
Smoking
16-20
(%) (30)
(%) (33)
Total
(6) (14) (10)
4 9 13
Table 3: Frequency Distribution of Smokers Duration
16.5
25.4
of Smokers
According to Lifetime
Exposure (cigarette/years) 200
_(%) ti_(%) Current smokers Former smokers Total Mean exposure
Total
63
(%) (100)
Mean exposure 158
25
(40)
25
(40)
13
(%) (20)
38
(57)
16
(24)
13
(19)
67
(100)
127
63
(48)
41
(32)
26
(20)
130
(100)
137
52
127
291 -
-
The frequency distributions of current smokers and forsmokers by cigarette consumption and smoking duration appear in Tables 2 and 3, respectively. Mean consumption was 9.9 and 11.2 cigarettes/day among current smokers and former smokers, respectively, and mean duration was 16.5 years and 10.8 years, respectively. The lifetime smoking exposure as derived from the product of the number of years of smoking and stated cigarette consumption (cigarette-years)17 for current smokers and former smokers is presented in Table 4. Comparison of bone height in different smoking exposure groups was performed after adjustment for differences in age using bone height in nonsmokers as reference. mer
(n 63) =
Sites
Maxillary
Mean 4.8 4.8 9.5
Non-smokers
Total
(n 80)
(n 143)
=
SEM
Mean
0.17 0.19 0.31
5.1 5.2 10.2
SEM 0.14 0.12 0.23
=
Mean 5.0
4.9 9.9
SEM 0.08 0.08 0.15
According to Cigarette
Consumption per Day Current smokers Former smokers Total
Smokers
Mandibular All
subjects.
Table 2:
243
The bite-wing radiograph represented the molar and premolar areas of the right side of the dentition. The distance from the cemento-enamel junction (CEJ) to the interdental septum (IS) was measured mesially and distally for all teeth from 14 to 17 and from 44 to 47. The mesial measurement of first premolare and the distal one of second molars were omitted. Thus a maximum of 12 sites representing 3 maxillary and 3 mandibular periodontal bone septa were available for measurement in each subject. The radiographs were read by one observer under a 7 x magnification and measurements were made to the nearest 0.1 mm. The observer performing the measurements was unaware of the smoking status of the individual subjects. The method and its precision of bone height measurements have been presented elsewhere.18 The measurability for the different predetermined sites varied from 71% to 88% with no systematic differences between smoking groups. The number of measurements included in the means of the subjects ("case-means") forming the maxillary, mandibular, and overall CEJ-IS values are presented in Table 5. Altogether, in 95% of subjects the overall case-mean was based on 6 or more site specific measurements. The presence of radiographically detectable calculus was examined on the same bite-wing radiographs for each proximal tooth surface corresponding to the interdental crest regions analyzed for bone height. Thus a maximum of 12 dental surfaces were examined in the subject. The habitual oral hygiene standard was evaluated in 19 individuals, selected at random, 8 smokers and 11 nonsmokers. The mean ± SEM age was 33.6 ± 2.15 years (range 25 to 42 years) in smokers and 36.7 ± 2.25 years (range 28 to 52 years) in non-smokers. Mean ± SD consumption among smokers was 15.0 ± 5.9 cigarettes/day. The plaque index was measured according to the method of Silness and Löe19 by one observer, unaware of the smoking status. The mean ( ± SEM) plaque index was 0.28 ± 0.03 and 0.33 ± 0.04 for smokers and non-smokers, respectively. The difference between the means was not sta-
tistically significant (/
=
1.07,
>
0.05).
Statistics Statistical significance of differences between means was tested by the Student r-distribution, two-tailed, or, if the variances differed, by Pitman's permutation test. Multiple regression analysis was carried out with the CEJ-IS distance as de-
244
J Periodontol April 1991
SMOKING AND BONE LOSS
MANDIBULAR SITES
CEJ-1S DISTANCE
(mm)
3.0
SMOKER EX-SMOKER
2.0
NON-SMOKER NON-SMOKER
1.0
Site 47/46
Site 46/45
Site 45/44
A MANDIBULAR SITES
regression of
Table 6: The CEJ-IS Distance and Cigarette Consumption
SMOKER EX-SMOKER
(mm)
10 Mean
10 Mean
SEM
1.51 2.71 2.06
0.157 0.407 0.205
Pitman's test >0.05
