Associations between smoking and tooth loss according to the reason for tooth loss: The Buffalo OsteoPerio

Study Xiaodan Mai, Jean Wactawski-Wende, Kathleen M. Hovey, Michael J. LaMonte, Chaoru Chen, Mine Tezal and Robert J. Genco JADA 2013;144(3):252-265
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Associations between smoking and tooth loss according to the reason for tooth loss
The Buffalo OsteoPerio Study
Xiaodan Mai, MBBS; Jean Wactawski-Wende, PhD; Kathleen M. Hovey, MS; Michael J. LaMonte, PhD, MPH; Chaoru Chen, PhD; Mine Tezal, DDS, PhD; Robert J. Genco, DDS, PhD

artial or total tooth loss has been associated with the onset of disability and mortality in the elderly.1 Although tooth loss in U.S. adults has decreased during the past few decades,2 tooth loss without replacement has been associated with a poor physical function index, as measured by the SF-36 Health Survey (QualityMetric, Lincoln, R.I.).3 Tooth loss also has been associated with chronic systemic conditions such as ischemic stroke,4 cancer,5 rheumatoid arthritis6 and diabetes.7 As a result, both partial and total tooth loss remain significant public health concerns in the United States. Understanding the reasons for tooth loss will facilitate the development of prevention strategies that, in turn, may benefit oral health and function and have a favorable effect on associated morbidities.

IN G

ED

Dr. Mai is a doctoral student in epidemiology, Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, The State University of New York. Dr. Wactawski-Wende is a professor, Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, The State University of New York, 270 Farber Hall, Buffalo, N.Y. 14214, e-mail jww@buffalo.edu. Address reprint requests to Dr. Wactawski-Wende. Ms. Hovey is a data analyst, Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, The State University of New York. Dr. LaMonte is an assistant professor, Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, The State University of New York. Dr. Chen is a former research support specialist, Department of Social and Preventive Medicine, School of Public Health and Health Professions, University at Buffalo, The State University of New York. Dr. Tezal is an assistant professor, Department of Oral Biology, School of Dental Medicine, University at Buffalo, The State University of New York. Dr. Genco is Distinguished Professor of Oral Biology and Microbiology, Department of Oral Biology, School of Dental Medicine, University at Buffalo, The State University of New York.

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Background. Smoking is associated with tooth loss. However, smokings relationship to the specific reason for tooth loss in postmenopausal women is unknown. A 1 RT I C LE Methods. Postmenopausal women (n = 1,106) who joined a Womens Health Initiative ancillary study (The Buffalo OsteoPerio Study) underwent oral examinations for assessment of the number of missing teeth, and they reported the reasons for tooth loss. The authors obtained information about smoking status via a self-administered questionnaire. The authors calculated odds ratios (ORs) and 95 percent confidence intervals (CIs) by means of logistic regression to assess smokings association with overall tooth loss, as well as with tooth loss due to periodontal disease (PD) and with tooth loss due to caries. Results. After adjusting for age, education, income, body mass index, history of diabetes diagnosis, calcium supplement use and dental visit frequency, the authors found that heavy smokers ( 26 pack-years) were significantly more likely to report having experienced tooth loss compared with never smokers (OR = 1.82; 95 percent CI, 1.103.00). Smoking status, packs smoked per day, years of smoking, pack-years and years since quitting smoking were significantly associated with tooth loss due to PD. For pack-years, the association for heavy smokers compared with that for never smokers was OR = 6.83 (95 percent CI, 3.40-13.72). The study results showed no significant associations between smoking and tooth loss due to caries. Conclusions and Practical Implications. Smoking may be a major factor in tooth loss due to PD. However, smoking appears to be a less important factor in tooth loss due to caries. Further study is needed to explore the etiologies by which smoking is associated with different types of tooth loss. Dentists should counsel their patients about the impact of smoking on oral health, including the risk of experiencing tooth loss due to PD. Key Words. Tooth loss; periodontal diseases; caries; smoking; menopause; womens health. JADA 2013;144(3):252-265.
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The U.S. Centers for Disease Control and Prevention, Atlanta, estimated the prevalence of current smoking among U.S. adults in 2007 to be 17.4 percent in women and 22.3 percent in men.8 Smoking has been associated with chronic illnesses such as respiratory ailments,9 cancer10 and heart disease.11 A positive association between smoking status and tooth loss has been indicated in several,12-27 but not all,28,29 published observational studies. Limitations in study design, including small sample size and incomplete adjustment for confounding variables, may explain in part the disparate findings between studies. In addition, few investigators have explored different reasons for tooth loss in relation to smoking habits, which also may explain inconsistencies in published results.30,31 Tooth loss can be a consequence of caries, periodontal disease (PD), accidents or trauma, previous root canal treatment, orthodontic procedures and other reasons. Caries and PD account for a large proportion of missing teeth in adult populations.32,33 Although caries is a major reason for tooth loss across all age groups, PD is a particularly important reason among older adults.34,35 Many studies pertaining to smoking and tooth loss were conducted in men, and fewer data are available regarding this association in women. Study results show that women often experience more tooth loss than men36,37 despite having better oral health practices and a lower smoking prevalence.8 Women older than 65 years have an average of 18.77 teeth, and the number of remaining teeth is 4.52 fewer among current smokers than it is among never smokers.38 In this study, we collected detailed information about cigarette smoking via selfadministered questionnaires, and we evaluated the extent of and reasons for tooth loss as part of a comprehensive oral examination in a large, well-characterized cohort of postmenopausal women. We then assessed the association between smoking and tooth loss and examined whether this association varied according to reasons for tooth loss in this study group.
METHODS

This cross-sectional study consisted of postmenopausal women enrolled in the Buffalo Osteoporosis and Oral Bone Loss (OsteoPerio) Study, which is ancillary to the Womens Health Initiative Observational Study (WHI OS)39,40 conducted at the Buffalo, N.Y., clinical center. Details about participant recruitment and selection have been described elsewhere.41 A total of 1,362 women completed the OsteoPerio visit. We restricted the current analyses to the 1,106

women for whom all information pertaining to the key study variables was available; these included a detailed smoking history, reason for tooth loss and the major confounding variables of interest. In addition, we excluded women from these analyses who had lost teeth owing to reasons other than caries or PD (Figure). The health sciences institutional review board at the University at Buffalo approved this study, and we obtained written informed consent from all participants before completing study assessments. Participants underwent a comprehensive oral examination administered by trained and calibrated dental examiners (M.T. and others) who used standardized protocols. We scheduled the OsteoPerio study visit to correspond approximately with the participants three-year WHI OS clinical visit. On examination, the dental examiner assessed the number of teeth present, the participant reported the reason for each missing tooth (excluding third molars) and the dental examiner recorded the reason for each missing tooth. Reasons for missing teeth included caries, PD, accident or trauma, orthodontic procedure, congenital absence, eruption problems, previous root canal treatment or unable to determine. The dental examiner classified participants as having no tooth loss if they had retained all 28 natural teeth (excluding third molars). Tooth loss. Among participants who were missing at least one tooth, the examiner categorized each missing tooth according to the womans self-reported reason it was missing. For these analyses, we defined those who reported at least one tooth missing as a result of PD as having tooth loss due to PD. We defined those reporting at least one tooth missing as a result of caries and no tooth loss as a result of PD as having tooth loss due to caries. We excluded from these analyses participants whose tooth loss was due only to reasons other than caries or PD (n = 113). We classified those without tooth loss as such. We conducted a validation study among a subsample of the OsteoPerio study population (n = 70), in which we contacted the participants personal dentists and asked them to report the reason for each missing tooth. We asked the dentists to refer to their patients dental records. They were not made aware of the participants self-reported reasons as part of the OsteoPerio study.
ABBREVIATION KEY. AP: Anteroposterior. BMI: Body mass index. PD: Periodontal disease. SES: Socioeconomic status. WHI OS: Womens Health Initiative Observational Study.
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Smoking. We obtained information about participants smoking habits from a Women Completing OsteoPerio Visit standardized self-adminis(n = 1,362) tered questionnaire completed during the OsteoPerio clinic visit. We categorized smoking status as never, former or current smokers on the basis of participants responses to Exclusion Criteria Applied this question: Do you use or (n = 1,196) have you used cigarettes now or in the past? We computed the number of years of smoking by subtracting the participants age at smoking initiation from her age at Participants for Whom Information smoking cessation for former About Confounding Variables smokers, and we subtracted Was Available the participants age at (n = 1,106) smoking initiation from her current age for current smokers. We computed smoking pack-years by multiplying the number of packs smoked per day (obtained from participants responses to No Tooth Loss Any Tooth Loss questions about packs smoked (n = 206) (n = 900) per day) by the number of years the participant smoked. We then classified participants into one of four categories: dnever smokers; Tooth Loss Tooth Loss dlight smokers (first tertile, Due to Due to < eight pack-years) Periodontal Disease Caries dmoderate smokers (second (n = 108) (n = 792) tertile, eight to 25 pack-years); dheavy smokers (third tertile, 26 pack-years). Figure. Flowchart of participants. Exclusion criteria (n = 166) included incomplete quesIn this study, cigarette tionnaires (n = 5), missing alveolar crestal height information (n = 16), missing reasons for tooth loss (n = 2), missing teeth due only to reasons other than periodontal disease or smoking was the predominant caries (n = 113) and missing information about pack-years of smoking (n = 30). source of tobacco exposure. Nine women reported using cigars, pipes or chewing tobacco, but these determined the participants age by using the women also reported smoking cigarettes. No date of birth. Participants described their race as data were available about the intensity or durawhite (not of Hispanic origin), black or African tion of use of tobacco products other than cigaAmerican (not of Hispanic origin), American rettes, and, therefore, we did not explore this Indian or Alaskan Native, Asian or Pacific information further in our analyses. Islander (ancestry is Chinese, Indo-Chinese, Participants characteristics. At the time of Korean, Japanese, Pacific Islander, Vietnamese), the study visit, we measured height and weight Hispanic/Latino (ancestry is Mexican, Cuban, according to standardized protocols. We calcuPuerto Rican, Central American or South lated body mass index (BMI) by dividing weight American) or other, and we then categorized them (in kilograms) by the square of height in meters. as white or other. We categorized educational In addition, we obtained data pertaining to other level into high school, college and graduate key variables from WHI OS questionnaires. We school. We categorized current annual family
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income as less than $35,000 or $35,000 or more. Questions regarding additional potential confounders included those pertaining to a history of diabetes diagnosis and medication use, hormone therapy, calcium and vitamin D supplement use and history of gingival surgery. We assessed participants oral health behaviors by using three variables: frequency of dental visits (> one per year versus one per year), frequency of toothbrushing ( two times per day versus < two times per day) and frequency of flossing (every day versus not every day). We assessed bone mineral density by means of dual-energy x-ray absorptiometry with use of a densitometer (QDR2000 densitometer, Hologic, Waltham, Mass.) at several body sites including the anteroposterior (AP) spine, femoral neck, total hip, wrist and total body. We converted bone mineral density values into T-scores for each of the skeletal sites.42 (The T-score is a comparison of a persons bone density with that of a healthy young adult [20 to 30 years old] of the same sex. It is a calculation of the standard deviations from the young adult mean value for that site.) We used the worst T-score from the measured sites, including the total hip, femoral neck, wrist, AP spine or total body to characterize a participants osteoporosis status. We further classified participants overall osteoporosis status as normal, low bone mass or osteoporosis according to World Health Organization diagnostic criteria.42,43 Data analysis. We compared characteristics of women retaining all 28 teeth with those of women who lost at least one tooth by using a t test for continuous variables and a 2 test for categorical variables. We selected confounding variables for the final models after assessing the contribution of each factor by itself after first adjusting for age. Our final adjusted models included age, education, BMI, history of diabetes diagnosis, calcium supplement use and dental visit frequency. We conducted logistic regression analyses to estimate the OR and 95 percent CI for the association between smoking history and overall tooth loss. To investigate whether the association differed according to the reason for tooth loss, we conducted separate logistic regression analyses stratified by those who lost any teeth due to PD and by those who lost any teeth due to caries (but none due to PD). In addition, we conducted analyses to assess whether the associations differed according to the severity of tooth loss (strata include loss of one to three teeth and more than three teeth specifically as a result of PD or caries). We examined the influence of smoking

intensity and duration by using the P for trend for continuous measures of packs smoked, years of smoking, pack-years of smoking, age at which participant started smoking, and years since participant quit smoking. We conducted sensitivity analyses that included only those women who had lost teeth due to PD exclusively (that is, excluding those with any tooth loss due to caries) (n = 47). In addition, we assessed effect modification by calcium supplement intake, vitamin D supplement intake and hormone therapy by adding cross-product interaction terms in logistic regression models. For the logistic regression analyses, we considered two-sided P values .05 to be statistically significant. We performed all analyses by using a statistical software package (SAS Version 9.2, SAS Institute, Cary, N.C.).
RESULTS

Characteristics. Participants characteristics are summarized in Table 1. Overall, the number of missing teeth ranged from 0 to 22. Two hundred six women retained all 28 teeth; 257, 297 and 346 women lost one to two teeth, three to five teeth and six or more teeth, respectively. The majority of study participants were white and had completed some college education. About one-half of participants reported never having smoked during their lifetime, whereas 16.5 percent were heavy smokers when classified according to pack-years of smoking. Twothirds of study participants reported having received menopausal hormone therapy, with slightly less than one-half reporting current use. More than two-thirds of women reported current use of a calcium supplement and more than one-half reported current use of a vitamin D supplement. When classified according to World Health Organization42,43 criteria, 48.6 percent of women had low bone mass and 25.5 percent had osteoporosis. Table 1 also presents selected characteristics according to tooth loss status. Factors significantly different according to tooth loss were age at the OsteoPerio clinic visit, BMI, educational level, annual family income, history of diabetes diagnosis, calcium supplement use, vitamin D supplement use, history of gingival surgery and dental visit frequency. Race, toothbrushing frequency and flossing frequency did not differ according to tooth loss status. We did not observe any significant differences for most smoking characteristics, including smoking status, packs smoked per day, years of smoking, pack-years of smoking, age at which participant started smoking and years since participant quit smoking.
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Smoking and tooth loss. Table 2 (page 258) presents results for crude, age-adjusted and multivariable-adjusted logistic regression analyses of smoking exposures and overall tooth loss. In the crude analyses, heavy smokers had significantly elevated odds of experiencing overall tooth loss compared with never smokers. This association was somewhat stronger after we controlled for age. Further adjustment for education, income, BMI, history of diabetes diagnosis, calcium supplement intake and dental visit frequency did not change the point or interval estimates appreciably. Packs smoked per day and pack-years of smoking, when measured as continuous variables, showed significant trends in multivariableadjusted models. When we measured them as categorical variables, the results showed no statistically significant associations between smoking status, packs smoked per day, years of smoking, age at which participant started smoking or years since quitting smoking and overall tooth loss. Reason for tooth loss. Next, we performed separate logistic regression analyses to relate
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Characteristics of 1,106 postmenopausal women overall and according to tooth loss status.
CHARACTERISTIC Missing Teeth, Mean (SD), No. Missing Teeth, No. (%) 0 1-2 3-5 6 Range Age at Visit, Mean (SD), in Years Smoking Status, No. (%) Never Former Current Packs Smoked per Day, No. (%) Never <1 1 to < 2 2 Years of Smoking, No. (%) Never < 16 16-30 31 Pack-Years, No. (%) Never Light (< 8 ) Moderate (8-25) Heavy ( 26) Age Started Smoking, Mean (SD), in Years Age Started Smoking, No. (%), in Years < 20 20 378 (73.7) 135 (26.3) 25.1 (13.1) 71 (79.8) 18 (20.2) 25.0 (12.2) 307 (72.4) 117 (27.6) 25.2 (13.3) .151 .907 593 163 173 177 593 161 170 182 18.3 (53.6) (14.7) (15.6) (16.0) (53.6) (14.6) (15.4) (16.5) (4.2) 117 34 29 26 117 34 32 23 17.7 (56.8) (16.5) (14.1) (12.6) (56.8) (16.5) (15.5) (11.2) (3.3) 476 129 144 151 476 127 138 159 18.5 (52.9) (14.3) (16.0) (16.8) (52.9) (14.1) (15.3) (17.7) (4.3) 593 (53.6) 270 (24.4) 188 (17.0) 55 (5.0) 117 (56.8) 52 (25.2) 30 (14.6) 7 (3.4) 476 (52.9) 218 (24.2) 158 (17.6) 48 (5.3) 593 (53.6) 473 (42.8) 40 (3.6) 117 (56.8) 81 (39.3) 8 (3.9) 476 (52.9) 392 (43.6) 32 (3.6) .541 206 257 297 346 (18.6) (23.2) (26.9) (31.3) (7.1) 63.8 (6.4) 0 257 (28.6) 297 (33.0) 346 (38.4) 1-22 67.6 (7.0) OVERALL NO TOOTH LOSS ANY TOOTH LOSS (N = 1,106)* (n = 206)* (n = 900)* 5.1 (5.6) 6.2 (5.6)

P VALUE

66.9

< .001

.441

.359

.142

.063

Years Since Quitting Smoking#, Mean (SD) Years Since Quitting Smoking,# No. (%) 30 20-29 10-19 < 10 * # **

182 117 105 69

(38.5) (24.7) (22.2) (14.6)

30 24 16 11

(37.0) (29.6) (19.8) (13.6)

152 93 89 58

(38.8) (23.7) (22.7) (14.8)

.722

Not all percentages total 100 percent because of rounding. P value calculated from a t test for continuous variables or a 2 test for categorical variables. SD: Standard deviation. Dash indicates not applicable. Restricted to former and current smokers (n = 513). Restricted to former smokers (n = 473). Included sites of total hip, femoral neck, wrist, anteroposterior spine or total body. Sources: World Health Organization42; Kanis and colleagues.43 kg/m2: Kilograms per square meter.

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CHARACTERISTIC Worst-Site T-Score,** No. (%) Normal Low bone mass Osteoporosis Race, No. (%) Other White Body Mass Index, Mean (SD), kg/m2 Education, No. (%) High School College Graduate school Annual Family Income, No. (%), $ < 35,000 35,000

OVERALL NO TOOTH LOSS ANY TOOTH LOSS (N = 1,106)* (n = 206)* (n = 900)*

P VALUE*

287 (26.0) 537 (48.6) 282 (25.5) 34 (3.1) 1,070 (96.9) 26.8 (5.2)

63 (30.6) 101 (49.0) 42 (20.4) 5 (2.4) 201 (97.6) 26.0 (4.5)

224 (24.9) 436 (48.4) 240 (26.7) 29 (3.2) 869 (96.8) 26.9 (5.4)

.096

.548 .015

252 (22.8) 493 (44.6) 361 (32.6)

22 (10.7) 101 (49.0) 83 (40.3)

230 (25.6) 392 (43.6) 278 (30.9)

< .001

466 (42.1) 640 (57.9)

51 (24.8) 155 (75.2)

415 (46.1) 485 (53.9)

< .001

History of Diabetes Diagnosis, No. (%) No Yes Ever Use Hormone Therapy, No. (%) No Yes Current Use of Hormone Therapy, No. (%) No Yes Use Calcium Supplement, No. (%) No Yes Use Vitamin D Supplement, No. (%) No Yes History of Gingival Surgery, No. (%) No Yes Brush Teeth < 2 times/day 2 times/day 259 (23.4) 847 (76.6) 43 (20.9) 163 (79.1) 216 (24.0) 684 (76.0) .339 866 (79.1) 229 (20.9) 173 (84.4) 32 (15.6) 693 (77.9) 197 (22.1) .038 476 (43.0) 630 (57.0) 76 (36.9) 130 (63.1) 400 (44.4) 500 (55.6) .048 324 (29.3) 782 (70.7) 47 (22.8) 159 (77.2) 277 (30.8) 623 (69.2) .024 608 (55.0) 498 (45.0) 105 (51.0) 101 (49.0) 503 (55.9) 397 (44.1) .201 370 (33.5) 736 (66.6) 58 (28.2) 148 (71.8) 312 (34.7) 588 (65.3) .074 1,050 (94.9) 56 (5.1) 202 (98.1) 4 (1.9) 848 (94.2) 52 (5.8) .024

Floss Teeth, No. (%) Not every day Every day Dental Visit 1 per year > 1 per year 271 (24.5) 835 (75.5) 35 (17.0) 171 (83.0) 236 (26.2) 664 (73.8) .006 626 (57.0) 473 (43.0) 119 (58.1) 86 (42.0) 507 (56.7) 387 (43.3) .727

smoking exposures with tooth loss due to PD and tooth loss due to caries as distinct outcome variables (Table 3, pages 260261). Of 900 women reporting loss of at least one tooth, 108 (12 percent) were classified as having experienced tooth loss due to PD and 792 (88 percent) were classified as having experienced tooth loss due to caries. In the crude analyses, ever smokers, packs smoked per day, duration of smoking, pack-years of smoking and years since quitting smoking all showed significantly increased odds of experiencing tooth loss due to PD when compared with findings in never smokers. After adjusting for age and other confounding variables, we found that these increased odds remained statistically significant. In the multivariableadjusted analyses, women who smoked two or more packs per day and those with the heaviest packyears of smoking exhibited a 10-fold and sevenfold elevated odds of experiencing tooth loss due to PD, respectively, when compared with findings in never smokers. We did not observe any clear relationship between age at which the participant
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Association between cigarette smoking and any tooth loss for 1,106 postmenopausal women.
CHARACTERISTIC NO TOOTH LOSS (n = 206), NO. (%)* ANY TOOTH LOSS (n = 900) No. (%) of Participants* Crude OR (95% CI) Age-Adjusted OR (95% CI) Multivariable-Adjusted OR (95% CI)

Smoking Status Analysis 1 Never Former Current Analysis 2 Never Ever Packs Smoked per Day Never <1 1 to < 2 2 P for trend P for trend# Years of Smoking Never < 16 16-30 31 P for trend P for trend# Pack-years Never Light (< 8) Moderate (8-25) Heavy ( 26) P for trend P for trend# Age Started Smoking# < 20 20 P for trend# Years Since Quitting Smoking** 30 20-29 10-19 < 10 P for trend# * # **

117 (56.8) 81 (39.3) 8 (3.9) 117 (56.8) 89 (43.2)

476 (52.9) 392 (43.6) 32 (3.6) 476 (52.9) 424 (47.1)

1.0 1.19 (0.87-1.63) 0.98 (0.44-2.19) 1.0 1.17 (0.86-1.59)

1.0 1.32 (0.96-1.83) 1.29 (0.57-2.93) 1.0 1.32 (0.97-1.81)

1.0 1.34 (0.96-1.86) 1.11 (0.47-2.58) 1.0 1.32 (0.95-1.82)

117 (56.8) 52 (25.2) 30 (14.6) 7 (3.4) 117 34 29 26 (56.8) (16.5) (14.1) (12.6) (56.8) (16.5) (15.5) (11.2)

476 (52.9) 218 (24.2) 158 (17.6) 48 (5.3) 476 129 144 151 (52.9) (14.3) (16.0) (16.8) (52.9) (14.1) (15.3) (17.7)

1.0 1.03 (0.72-1.48) 1.30 (0.83-2.01) 1.69 (0.74-3.82) .141 .271 1.0 0.93 (0.61-1.43) 1.22 (0.78-1.91) 1.43 (0.90-2.27) .099 .158 1.0 0.92 (0.60-1.41) 1.06 (0.69-1.64) 1.70 (1.05-2.75) .041 .063

1.0 1.11 (0.77-1.62) 1.53 (0.97-2.40) 2.05 (0.89-4.71) .026 .135 1.0 1.18 (0.76-1.83) 1.35 (0.85-2.13) 1.47 (0.91-2.35) .102 .628 1.0 1.08 (0.70-1.68) 1.18 (0.75-1.84) 1.87 (1.14-3.05) .020 .088

1.0 1.14 (0.78-1.67) 1.49 (0.94-2.35) 1.90 (0.82-4.50) .050 .210 1.0 1.16 (0.74-1.83) 1.40 (0.88-2.24) 1.41 (0.87-2.29) .123 .757 1.0 1.10 (0.70-1.72) 1.18 (0.75-1.87) 1.82 (1.10-3.00) .039 .158

117 34 32 23

476 127 138 159

71 (79.8) 18 (20.2)

307 (72.4) 117 (27.6)

1.0 1.50 (0.86-2.63) .114

1.0 1.11 (0.62-1.99) .517

1.0 1.12 (0.62-2.04) .545

30 24 16 11

(37.0) (29.6) (20.0) (13.6)

152 93 89 58

(38.8) (23.7) (22.7) (14.8)

1.0 0.77 (0.42-1.39) 1.10 (0.57-2.13) 1.04 (0.49-2.21) .906

1.0 0.90 (0.48-1.65) 1.24 (0.63-2.44) 1.24 (0.57-2.68) .452

1.0 0.89 (0.47-1.67) 1.22 (0.61-2.45) 1.24 (0.56-2.73) .503

Not all percentages total 100 percent because of rounding. OR: Odds ratio. CI: Confidence interval. Adjusted for age, education, income, body mass index, history of diabetes diagnosis, calcium supplement use and dental visit frequency. Included all participants. Restricted to former and current smokers (n = 513). Restricted to former smokers (n = 473).

started smoking and tooth loss due to PD. We did find a significant inverse trend between years since quitting smoking and reported tooth loss due to PD (P trend < .01). There was no clear association between smoking variables and tooth loss due to caries in crude, ageadjusted or multivariable-adjusted models.
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Increasing numbers of packs smoked per day and duration of cigarette smoking showed slightly increased odds of experiencing tooth loss due to caries; however, neither of these associations reached statistical significance. We further assessed whether the association between cigarette smoking and tooth loss dif-

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fered according to the severity of tooth loss, as indicated by the reported number of teeth lost due to PD and the reported number of teeth lost due to caries as separate outcomes (Table 4, page 262). The patterns of association between smoking exposures and severity of tooth loss for either reason (PD or caries) were similar to those in Table 3. The results of additional analyses showed that there was no evidence of effect modification of the association between smoking and tooth loss according to calcium supplement intake, vitamin D supplement intake or hormone therapy (data not shown). Last, we conducted sensitivity analyses for PD restricted to participants with tooth loss due exclusively to PD. The point estimates and patterns of association with smoking exposures were similar to those presented in Table 3 (data not shown).
DISCUSSION

To our knowledge, this study is the first to evaluate the association between several smoking exposure variables and tooth loss prevalence according to the specific reason for tooth loss among a cohort of postmenopausal women. The availability of smoking exposure variables in the OsteoPerio study was more extensive than that in most previous studies. In our cohort, heavy smokers ( 26 pack-years of smoking) had significantly higher odds of experiencing tooth loss compared with never smokers (OR = 1.82; 95 percent CI, 1.10-3.00) after we controlled for age, education, income, BMI, history of diabetes diagnosis, calcium supplement use and frequency of dental visits. This result is in accordance with those of previous studies in which investigators observed a dose-response relationship between cigarette smoking and tooth loss.12,13,44-48 Moreover, former smokers were at higher odds of experiencing tooth loss compared with never smokers, although this association was of borderline statistical significance in our study (OR = 1.34; 95 percent CI, 0.96-1.86). Investigators in other studies have reported inconsistent associations between former smoking and overall tooth loss.12,14-21 In our study, current smokers did not have higher odds of experiencing tooth loss compared with never smokers, which is in contrast with the results of the majority of reports in the literature, which show a wide range (from 1.7 to 4.7) in effect size estimates (OR or risk ratio).12-27 However, it is important to note that the prevalence of current smoking in our study tended to be lower than that reported in other cohorts of women, and

this could account in part for the discrepant findings. Differences in study populations and in methodologies for defining key variables may provide a partial explanation of the disparate results. Our sample consisted entirely of postmenopausal women who generally were healthy and reported practicing good oral hygiene. Men are more likely than women to smoke and to be heavy smokers, and the effect of smoking on tooth loss may be stronger in men than it is in women.27 The prevalence of current smokers was relatively low (3.6 percent) in our cohort, and all participants were required to have at least six teeth at study entry.41 Some previous studies22-26 have included edentulous participants, who also were more likely than participants in our study to have been heavy smokers. The small proportion of current and heavy smokers may have limited the statistical power of our study to detect stronger and more consistent associations between smoking status and tooth loss. When stratified according to reason for tooth loss, nearly all of the smoking exposure variables were strongly and consistently associated with tooth loss due to PD. In contrast, none of the smoking exposure variables were associated with tooth loss due to caries. Thus, a null relationship between smoking and overall tooth loss in postmenopausal women may be explained by the limited effect of smoking on tooth loss due to caries in previous studies. The etiology of the effect of smoking on tooth loss may explain further the large range of effect sizes that have been reported in the literature.12-27 Although caries is a common reason for tooth loss in all age groups, the frequency of tooth loss due to PD increases with age.35,49 Hence, the effect of smoking on tooth loss due to PD may be weaker in studies consisting mostly of young adults, which could further attenuate the point estimate between smoking exposures and overall tooth loss, PD and caries combined. To our knowledge, researchers in only one study conducted in Bangladesh investigated smoking as a risk factor for tooth loss due to PD and caries separately, and they reported similar results.31 However, tooth extraction practices in Bangladesh may differ from those in the United States, which might result in systematically different reasons for tooth loss across studies. In addition, data in the Bangladesh study were collected only for tooth loss occurring in populations of low socioeconomic status (SES) within 45 days of the dental visit, so these results should be interpreted with caution.
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Association between cigarette smoking and tooth loss due to periodontal disease and caries for 1,106 postmenopausal women.
CHARACTERISTIC NO TOOTH LOSS, TOOTH LOSS DUE TO PERIODONTAL DISEASE (n = 108) NO. (%) OF No. (%) of Crude OR Age-Adjusted Multivariable-Adjusted PARTICIPANTS (95% CI) Participants* OR (95% CI) OR (95% CI) (n = 206)*

Smoking Status Analysis 1 Never Former Current Analysis 2 Never Ever Packs Smoked per Day Never <1 1 to < 2 2 P for trend P for trend# Years of Smoking Never < 16 16-30 31 P for trend P for trend# Pack-Years Never Light (< 8) Moderate (8-25) Heavy ( 26) P for trend P for trend# Age Started Smoking,# Years < 20 20 P for trend# Years Since Quitting Smoking** 30 20-29 10-19 < 10 P for trend# *

117 (56.8) 81 (39.3) 8 (3.9) 117 (56.8) 89 (43.2)

36 (33.3) 63 (58.3) 9 (8.3) 36 (33.3) 72 (66.7)

1.0 2.53 (1.54-4.16) 3.66 (1.31-10.17) 1.0 2.63 (1.62-4.27)

1.0 2.83 (1.66-4.80) 5.33 (1.82-15.61) 1.0 3.02 (1.80-5.06)

1.0 2.99 (1.70-5.23) 4.07 (1.27-13.03) 1.0 3.09 (1.78-5.34)

117 (56.8) 52 (25.2) 30 (14.6) 7 (3.4)

36 29 31 12

(33.3) (26.9) (28.7) (11.1)

1.0 1.81 (1.01-3.26) 3.36 (1.80-6.28) 5.57 (2.04-15.21) < .001 .015

1.0 1.98 (1.06-3.69) 3.81 (1.96-7.43) 8.64 (2.98-25.10) < .001 .005

1.0 2.24 (1.15-4.37) 3.17 (1.56-6.45) 10.39 (3.41-31.68) < .001 .006

117 34 29 26

(56.8) (16.5) (14.1) (12.6) (56.8) (16.5) (15.5) (11.2)

36 (33.3) 8 (7.4) 26 (24.1) 38 (35.2) 36 13 16 43 (33.3) (12.0) (14.8) (39.8)

1.0 0.77 (0.33-1.80) 2.91 (1.52-5.57) 4.75 (2.55-8.56) < .001 < .001 1.0 1.24 (0.59-2.61) 1.63 (0.80-3.30) 6.08 (3.24-11.40) < .001 < .001

1.0 1.02 (0.42-2.50) 3.15 (1.60-6.20) 4.98 (2.59-9.58) < .001 .001 1.0 1.50 (0.69-3.29) 1.68 (0.80-3.56) 7.15 (3.66-13.97) < .001 < .001

1.0 1.17 (0.46-2.96) 3.31 (1.60-6.82) 4.64 (2.34-9.23) < .001 .008 1.0 1.60 (0.70-3.66) 1.71 (0.77-3.80) 6.83 (3.40-13.72) < .001 < .001

117 34 32 23

71 (79.8) 18 (20.2)

52 (72.2) 20 (27.8)

1.0 1.52 (0.73-3.15) 0.452

1.0 1.12 (0.51-2.46) 0.963

1.0 1.16 (0.48-2.78) 0.838

30 24 16 11

(37.0) (29.6) (19.8) (13.6)

13 15 19 16

(20.6) (23.8) (30.2) (25.4)

1.0 1.44 (0.58-3.61) 2.74 (1.08-6.95) 3.36 (1.23-9.18) .009

1.0 2.04 (0.76-5.48) 3.48 (1.27-9.51) 4.36 (1.48-12.81) .002

1.0 2.11 (0.73-6.06) 3.08 (1.02-9.29) 4.55 (1.43-14.42) .008

Not all percentages total 100 percent because of rounding. OR: Odds ratio. CI: Confidence interval. ORs adjusted for age, education, income, body mass index, history of diabetes diagnosis, calcium supplement use and dental visit frequency. Included all participants. # Restricted to former and current smokers (n = 513). ** Restricted to former smokers (n = 473).

Cigarette smoking could accelerate the course of PD. The results of previous studies suggest that the chemicals found in smoke select for plaque-forming anaerobic bacteria that may
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modify the oral microflora50 and decrease the antioxidative capacity of saliva.51 Free radicals produced by the host during the immune response to bacterial stimulation then damage

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be lower in smokers than in nonsmokers,55 and this effect may be particularly deleterious among postmenopausal women. TOOTH LOSS DUE TO CARIES (n = 792) In this study, we did not observe an association between smoking No. (%) of Crude OR Age-Adjusted MultivariableParticipants (95%CI) OR (95% CI) Adjusted and tooth loss due to caries. PreOR (95% CI) vious research findings suggest that smoking may increase the risk of developing dental caries by 440 (55.6) 1.0 1.0 1.0 impairing salivary function and 329 (41.5) 1.08 (0.79-1.48) 1.21 (0.87-1.67) 1.22 (0.87-1.70) 23 (2.9) 0.76 (0.33-1.75) 1.02 (0.44-2.39) 0.91 (0.38-2.18) salivary buffering capacity.56 However, tooth loss due to caries may 440 (55.6) 1.0 1.0 1.0 not be directly related to smoking, 352 (44.4) 1.01 (0.77-1.33) 1.19 (0.87-1.64) 1.19 (0.86-1.65) but may be influenced by factors such as SES and access to, and utilization of, dental care.57 Teeth with 440 (55.6) 1.0 1.0 1.0 dental caries are restorable given 189 (23.9) 0.97 (0.67-1.40) 1.04 (0.71-1.51) 1.05 (0.72-1.55) 127 (16.0) 1.13 (0.72-1.76) 1.38 (0.87-2.19) 1.38 (0.86-2.21) that dental care is accessible and 36 (4.6) 1.37 (0.59-3.15) 1.57 (0.67-3.68) 1.41 (0.59-3.39) utilized. Therefore, tooth loss may .503 .141 .220 not be the end result. On the other .528 .300 .428 hand, periodontitis, once developed, tends to be persistent. Effective treatment of periodontitis, 440 (55.6) 1.0 1.0 1.0 121 (15.3) 0.95 (0.62-1.46) 1.19 (0.76-1.85) 1.15 (0.72-1.81) which is based on control of both 118 (14.9) 1.08 (0.69-1.71) 1.19 (0.75-1.90) 1.25 (0.78-2.01) dental biofilm and inflammation, is 113 (14.3) 1.16 (0.72-1.85) 1.20 (0.74-1.94) 1.17 (0.71-1.92) more difficult to achieve.58 Thus, .556 .540 .537 periodontitis may lead to tooth loss .586 .736 .729 more often in older populations. Smoking cessation and PD. 440 (55.6) 1.0 1.0 1.0 Smoking cessation may prevent PD 114 (14.4) 0.89 (0.58-1.38) 1.04 (0.66-1.62) 1.05 (0.66-1.65) 122 (15.4) 1.01 (0.65-1.57) 1.13 (0.72-1.78) 1.14 (0.72-1.81) from progressing to tooth loss. 116 (14.7) 1.34 (0.82-2.19) 1.49 (0.90-2.47) 1.46 (0.87-2.44) Researchers in several studies have .326 .189 .273 investigated the associations of .317 .386 .522 smoking cessation with PD59,60 and tooth loss.61,62 However, to our knowledge, investigators have not 255 (72.4) 1.0 1.0 1.0 studied the influence of smoking 97 (27.6) 1.50 (0.85-2.65) 1.14 (0.63-2.05) 1.16 (0.63-2.13) 0.08 0.36 0.35 behavior on specific reasons for tooth loss (caries or PD), and published findings specifically in postmenopausal women are not avail139 (42.3) 1.0 1.0 1.0 able, to our knowledge. Some 78 (23.7) 0.70 (0.38-1.28) 0.83 (0.45-1.55) 0.82 (0.43-1.55) 70 (21.3) 0.94 (0.48-1.85) 1.06 (0.54-2.11) 1.08 (0.53-2.19) researchers have addressed the role 42 (12.8) 0.82 (0.38-1.78) 0.99 (0.45-2.20) 1.01 (0.45-2.29) of smoking cessation. Investigators .418 .962 .913 conducting a study with use of National Health and Nutrition the periodontium, increasing the persons susExamination Survey III data reported that the ceptibility to tooth loss due to PD. Another odds of periodontitis developing declined with the mechanism by which cigarette smoking may reported number of years since smoking cessaaffect PD progression is toxic effects on bone. tion.59 The findings of the U.S. Health ProfesStudy results have shown that nicotine reduces sionals Follow-Up Study showed that risk of selfbone density and bone mineral content through reported tooth loss among middle-aged and older an increased secretion of bone-resorbing factors52 men decreased after smoking cessation, though it or a decreased intestinal uptake of calcium.53 remained elevated by 20 percent even 10 or more Estrogen may attenuate osteoporotic bone loss.54 years after participants quit smoking compared Estrone and estradiol levels have been shown to with the risk among never smokers.61 Consistent
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women in the States. Adjusted* ORs and 95 percent CIs for the associations United Study limitabetween cigarette smoking and severity of tooth loss tions. Our study had several limitadue to periodontal disease and caries. tions that one VARIABLE ADJUSTED OR (95% CI) should consider Tooth Loss Due Tooth Loss Due to Caries when interpreting to Periodontal Disease its findings. First, 1 to 3 teeth More than 3 1 to 3 teeth More than 3 causal relation(n = 53) teeth (n = 55) (n = 394) teeth (n = 398) ships cannot be Smoking Status inferred from the Never 1.0 1.0 1.0 1.0 cross-sectional data Former 3.05 (1.51-6.19) 3.13 (1.49-6.57) 1.28 (0.89-1.84) 1.13 (0.76-1.68) Current 5.04 (1.29-19.77) 3.00 (0.62-14.40) 0.56 (0.18-1.71) 1.50 (0.56-4.00) reported here. However, although Packs Smoked per Day we could not deterNever 1.0 1.0 1.0 1.0 mine whether all <1 2.67 (1.19-5.99) 1.70 (0.66-4.30) 1.13 (0.75-1.72) 0.98 (0.62-1.56) tooth loss occurred 1 to < 2 3.00 (1.19-7.57) 4.00 (1.65-9.70) 1.36 (0.82-2.27) 1.36 (0.79-2.34) after smoking expo2 10.80 (2.88-40.50) 11.26 (2.66-47.71) 1.33 (0.50-3.52) 1.68 (0.63-4.51) sure, we measured P for trend < .001 < .001 .341 .186 P for trend .022 .024 .697 .217 the duration of smoking cessation Years of Smoking Never 1.0 1.0 1.0 1.0 and our findings < 16 0.78 (0.20-3.11) 1.67 (0.52-5.36) 1.45 (0.90-2.35) 0.76 (0.42-1.36) suggest that 16-30 3.72 (1.55-8.91) 2.95 (1.14-7.64) 1.16 (0.69-1.95) 1.35 (0.78-2.33) smoking cessation 31 4.98 (2.18-11.39) 4.53 (1.82-11.24) 1.00 (0.57-1.75) 1.44 (0.82-2.53) is associated with P for trend < .001 < .001 .926 .167 significantly lower P for trend .009 .126 .134 .190 odds of experiPack-years encing tooth loss Never 1.0 1.0 1.0 1.0 Light (< 8) 1.19 (0.38-3.72) 2.08 (0.73-5.95) 1.23 (0.76-2.00) 0.82 (0.46-1.43) due to PD. A second Moderate (8-25) 2.44 (0.96-6.19) 1.10 (0.33-3.63) 1.12 (0.68-1.85) 1.16 (0.68-1.99) limitation is that Heavy ( 26) 7.07 (3.04-16.41) 7.59 (3.05-18.90) 1.36 (0.77-2.39) 1.65 (0.93-2.95) the study cohort P for trend < .001 < .001 .621 .115 consisted mostly of P for trend .001 .004 .887 .133 white women of Age Started higher SES who Smoking, Years had good oral < 20 1.0 1.0 1.0 1.0 20 0.69 (0.22-2.18) 2.19 (0.74-6.50) 1.13 (0.58-2.19) 1.17 (0.58-2.35) hygiene; the perP for trend .295 .068 .326 .534 centage of current Years Since Quitting smokers was low. Smoking# This could limit 30 1.0 1.0 1.0 1.0 generalizability 20-29 2.13 (0.58-7.86) 2.14 (0.52-8.79) 0.58 (0.29-1.20) 1.23 (0.57-2.64) and comparison of 10-19 2.80 (0.72-10.94) 3.58 (0.84-15.13) 0.78 (0.36-1.69) 1.86 (0.79-4.38) < 10 4.95 (1.25-19.59) 4.97 (1.08-22.95) 0.81 (0.34-1.93) 1.46 (0.53-3.92) our results with P for trend# .018 .044 .414 .213 those in cohorts * Adjusted for age, education, income, body mass index, history of diabetes diagnosis, calcium supplement that included more use and dental visit frequency. The reference group was women who retained all 28 natural teeth current smokers or (excluding third molars). groups of greater OR: Odds ratio. CI: Confidence interval. ethnic or SES Included all participants. diversity. Restricted to former and current smokers (n = 513). # Restricted to former smokers (n = 473). Validation study. The reasons with these results, our findings of moderate to for tooth loss in this study were self-reported. strong positive associations between smoking We conducted a validation study in a subset of exposures and tooth loss due to PD suggest that the OsteoPerio cohort (n = 70) in which the smoking cessation and smoking prevention proactual prevalence of tooth loss due to PD and grams potentially could reduce tooth loss due to that due to caries was 34 and 54 percent, PD in the growing population of postmenopausal respectively, as determined by a review of the
TABLE 4

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participants dental record by her personal dentist (via a mailed questionnaire). Results of this validation study showed that most self-reports of not having experienced tooth loss due to PD were confirmed by the participants personal dentists (43 of 59 dentists; negative predictive value = 72.9 percent). Likewise, the majority of self-reports of having experienced tooth loss due to PD were confirmed by participants personal dentists (eight of 11 dentists; positive predictive value = 72.7 percent). Given the relatively small number of false-positive reports of tooth loss due to PD, the findings of this validation study also indicated that the reason for tooth loss was self-reported with high specificity (93.5 percent). Conversely, we observed low sensitivity (33.3 percent) of self-reported tooth loss due to PD, owing to a relatively high proportion of falsenegative values. This finding indicates that women in our study underreported PD as the reason for their tooth loss, perhaps in part because caries also affected the tooth, and the discussion about caries with the dentist, the treatment of caries or both may have been recalled more clearly by participants than was a diagnosis of PD in the same tooth. As a result, our findings regarding the association between smoking habits and PD could be underestimated, and findings pertaining to the role of smoking in tooth loss due to caries may be overestimated because they include some tooth loss due to PD. Most self-reports of tooth loss due to caries were confirmed by participants personal dentists (37 of 58 dentists; positive predictive value = 63.8 percent). Nonetheless, there were a sizable number of falsepositive findings, resulting in low specificity (34.4 percent) of reported tooth loss due to caries. Among women who reported no tooth loss due to caries, the number of false-negative findings was small (one of 12), which resulted in high values for both sensitivity (97.4 percent) and negative predictive value (91.7 percent). Collectively, the validation study findings indicate that the reported associations between smoking habits and tooth loss may be biased toward the null hypothesis. Thus, the strong association between smoking and tooth loss specifically due to PD would not be expected to be changed in the study. Several study strengths add relevance to the current literature pertaining to smoking and tooth loss. These include the following: da relatively large study group compared with those of previous studies; dan entirely postmenopausal cohort of older women in whom the burden of poor oral health

and the need for improved prevention and control opportunities will challenge public health and clinical periodontology increasingly in coming years; ddental assessment information collected during comprehensive standardized oral examinations by trained dental examiners who could verify which teeth were missing; devaluation of several smoking exposure variables typically not available in previous epidemiologic studies of this issue; dthe availability of information about several individual and clinical factors that could be evaluated as potential confounding effects on the observed association between smoking and tooth loss. To our knowledge, this is one of the most comprehensive examinations of smoking and tooth loss; these are the only available findings in a large, well-characterized cohort of postmenopausal women who were not selected on the basis of PD or through clinical periodontal catchments.
CONCLUSIONS

These study findings suggest that there is an association between cigarette smoking and tooth loss in postmenopausal women, and this association primarily is the result of tooth loss due to PD. Investigators in previous studies who did not examine the role of smoking according to the reason for tooth loss may have underreported the importance of smoking in tooth loss, especially tooth loss due to PD. Researchers in future studies should investigate the reasons for tooth loss in older adults when considering smoking as a risk factor. Our findings suggest that smoking prevention and control could be important facets of comprehensive targeted strategies to control PD and its oral health complications in the growing population of postmenopausal women in the United States. I
Disclosure. None of the authors reported any disclosures. This study was supported by grant R01DE013505 from the National Institute of Dental and Craniofacial Research, National Institutes of Health (NIH), Bethesda, Md., to Dr. Wactawski-Wende, U.S. Army, Medical Research and Materiel Command, Fort Detrick, Md., grant OS950077 and NIH/National Heart Lung and Blood Institute contracts N01WH32122 and HHSN268201100001C (Womens Health Initiative) to Dr. Wactawski-Wende. 1. Holm-Pedersen P, Schultz-Larsen K, Christiansen N, Avlund K. Tooth loss and subsequent disability and mortality in old age (published online ahead of print Jan. 5, 2008). J Am Geriatr Soc 2008; 56(3):429-435. doi:10.1111/j.1532-5415.2007.01602.x. 2. Dye BA, Tan S, Smith V, et al. Trends in oral health status: United States, 1988-1994 and 1999-2004. Vital Health Stat 11 2007 (248):1-92. 3. Mack F, Schwahn C, Feine JS, et al. The impact of tooth loss on general health related to quality of life among elderly Pomeranians:

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