- Email: [email protected]
Third Molars and Periodontal Pathologic Findings in Middle-Age and Older Americans
J Oral Maxillofac Surg 67:2592-2598, 2009
Third Molars and Periodontal Pathologic Findings in Middle-Age and Older Americans Kevin L. Moss,* Esther S. Oh, DDS, MD,† Elda Fisher, DMD,‡ James D. Beck, PhD,§ Steven Offenbacher, DDS, PhD,¶ and Raymond P. White, Jr, DDS, PhD储 Purpose: To assess the association between the visible presence of third molars and the severity of
periodontal pathologic findings on teeth more anterior in the mouth. Patients and Methods: The present analysis included dentate participants, 52 to 74 years old, from the
Dental Atherosclerosis Risk in Communities study who had undergone an oral examination that included periodontal probing depths (PDs) on all visible teeth, including any third molars. A PD of 4 mm or more and a clinical attachment level of 3 mm or greater were indicator variables for periodontal pathologic features. Explanatory variables were the presence or absence of visible third molars. The covariates included gender, ethnicity, age, income level, education, and smoking status. The outcome variables for periodontal pathologic features were the mean PD, extent (percentage of probing sites) of PDs of 4 mm or more, and the extent (percentage of probing sites) of a clinical attachment level of 3 mm or more. The outcomes between those with and without visible third molars were compared using descriptive statistics and chi-square tests, with significance set at P ⫽ .05. Multivariate modeling was performed using Statistical Analysis Systems SAS Proc GLM (SAS Institute, Cary, NC) to calculate the least squared means, adjusting for the study outcome variables and covariates. Results: The Dental Atherosclerosis Risk in Communities study sample included 6,793 subjects; 80% were white and 19% were black. Most (53%) were 62 to 74 years old and female (54%). Of the 6,793 participants, 2,035 (30%) had at least 1 visible third molar. The presence of a visible third molar was significantly associated with male gender, black race, age younger than the mean of 62.4 years, greater income, and never smoking (all P ⬍ .01). A greater mean PD for the first and second molars, the extent of PD of 4 mm or more at the first and second molars, and the extent of a clinical attachment level of 3 mm or more at the first and second molars were all significantly associated with the presence of a visible third molar in the unadjusted and adjusted models. Conclusions: In these middle-age and older Americans, the presence of a visible third molar was significantly associated with more severe periodontal disease on teeth more anterior in the mouth compared with those subjects with no visible third molars. © 2009 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 67:2592-2598, 2009
Received from the University of North Carolina School of Dentistry, Chapel Hill, NC. *Research Specialist, Department of Dental Ecology. †Resident, Department of Oral and Maxillofacial Surgery. ‡Resident, Department of Oral and Maxillofacial Surgery. §Kenan Distinguished Professor, Associate Dean for Research, Department of Dental Ecology. ¶OraPharma Distinguished Professor, Department of Periodontology. 储Dalton L. McMichael Distinguished Professor, Department of Oral and Maxillofacial Surgery. The Atherosclerosis Risk in Communities Study was performed as a collaborative study supported by National Heart,
Lung, and Blood Institute grants N01-HC-55015, N01-HC-55016, N01-HC-55018, N01-HC-55019, N01-HC-55020, N01-HC-55021, and N01-HC-55022. The present analyses were supported by National Institute of Dental and Craniofacial Research grant R01DE 11551. Grant support provided by the OMS Foundation, AAOMS. Address correspondence and reprint requests to Dr White: Department of Oral and Maxillofacial Surgery, University of North Carolina School of Dentistry, CB 7450, Chapel Hill, NC 27559-7450; e-mail: [email protected] © 2009 American Association of Oral and Maxillofacial Surgeons
0278-2391/09/6712-0007$36.00/0 doi:10.1016/j.joms.2009.04.046
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Clinicians are hampered in providing advice to their patients about the management of third molars because few population data exist from the United States on the presence or absence of third molars, and third molars are often not included in clinical studies of periodontal inflammatory disease. Elter et al1 reported a significant association between identifying a visible third molar and the periodontal health of an adjacent second molar in the dentate subjects with an average age of 62 years from the Dental Atherosclerosis Risk in Communities (DARIC) study. A visible third molar was associated with 1.5 times the odds of detecting at least 1 periodontal probing depth (PD) of 5 mm or more or bleeding on probing of the adjacent second molar, controlling for other factors associated with the visible presence of third molars and periodontal disease. Their report did not assess periodontal disease affecting third molars nor the severity of periodontal disease of DARIC subjects on teeth anterior to the second molars. From an older population in North Carolina with an average age of 73 years, Moss et al2 reported that 42% of dentate subjects had at least 1 third molar and 14% subjects had 4 third molars. Periodontal disease was not exclusive to the third molars in this population of senior adults. If teeth more anterior to third molars were not affected, fewer than 1% subjects had at least 1 third molar clinical attachment level (CAL) of 3 mm or more, and only 8% of subjects had at least 1 third molar PD of 4 mm or more. The relationship between the visible presence of third molars versus no visible third molars and patients’ periodontal disease level was not reported. The present study was designed to further our understanding of the association between retained third molars and periodontal inflammatory disease by studying the population of DARIC subjects to document the presence or absence of visible third molars and assess the association between the visible presence of third molars and the severity of periodontal pathologic findings on teeth more anterior than third molars using commonly applied measures of periodontal inflammatory disease, including the mean PD, extent (percentage of sites) of PD of 4 mm or more, and extent (percentage of sites) of CAL of 3 mm or more.
sites, with data collected from 1996 to 1998. The cross-sectional study included all dentate Atherosclerosis Risk in Communities participants aged 52 to 74 years who had undergone a periodontal examination. Those with a medical contraindication to periodontal probing were excluded. The DARIC oral examination was conducted by trained, calibrated examiners and included the periodontal PDs, 6 sites per tooth, for all visible teeth, including the third molars. No radiographs were available to complement the clinical examinations. Additional details of the DARIC study are provided in the report by Beck et al.4 The participants’ mean PD, PD of 4 mm or more, and CAL of 3 mm or more at the third molars and more anterior teeth were considered indicator variables for periodontal pathologic features. For our analyses, the DARIC participants were divided into 2 groups according to the presence of at least 1 visible third molar versus no visible third molar, main explanatory variables. Covariates included gender, ethnicity/race (black or white), age, income level per year (less than $25K, $25 to 50K, and more than $50K), level of education (basic [less than high school], intermediate [high school graduate], and advanced [more than high school]), and smoking status (current, former, or never). The outcome variables for the subjects’ level of periodontal pathologic disease were the mean periodontal PD, the mean extent (percentage of probing sites) with a PD of 4 mm or more, and the mean extent (percentage of probing sites) with a CAL of 3 mm or more. The outcomes between those with and without a visible third molar were compared using descriptive statistics and chi-square or t tests, with statistical significance set at P ⫽ .05. The potential confounders of ethnicity by study center, gender, smoking, age, education, and income were added to the adjusted models according to their association with the visible presence or absence of a third molar. Multivariable modeling was performed using Statistical Analysis Systems SAS Proc GLM (SAS Institute, Cary, NC) to calculate the least squared means, adjusting for outcome variables and covariates.
Results Patients and Methods The DARIC study, an institutional review board-approved substudy of the Atherosclerosis Risk in Communities Study, targeted 4 sites in the United States: Forsyth County, North Carolina; Jackson, Mississippi; suburbs of Minneapolis, Minnesota; and Washington County, Maryland.3 The oral examination involved participants at the Atherosclerosis Risk in Communities’ 4
The mean age of the 6,793 DARIC participants was 62.4 ⫾ 5.6 years. More of the participants were women (54%); 80% were white and 19% were black. Of the 6,793 participants, 86% had at least a high school education and 43% had been educated beyond high school. More than one half of the subjects were current (12%) or former (39%) smokers, and 14% of all participants had been diagnosed with diabetes melli-
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Table 1. CHARACTERISTICS OF DENTAL ATHEROSCLEROSIS RISK IN COMMUNITIES’ PARTICIPANTS (n ⴝ 6,793; 4,758 HAD NO VISIBLE THIRD MOLARS, 2,035 HAD AT LEAST 1 VISIBLE THIRD MOLAR)
Third Molar Visible Characteristic
No
Yes
Race Black White
819 (65.0) 3,865 (70.9)
441 (35.0) 1,588 (29.1)
Gender Female Male
2,764 (75.6) 1,932 (62.7)
894 (24.4) 1,148 (37.3)
Mean age (yr)
62.8 ⫾ 5.66
61.6 ⫾ 5.47
Education level Less than high school (0-ⱕ11 yr) High school graduate (12-16 yr) More than high school (ⱖ17 yr)
P Value ⬍ .0001
⬍ .0001
⬍ .0001 .04
662 (73.1)
244 (26.9)
2,023 (69.8)
877 (30.2)
2,005 (68.6)
918 (31.4)
Income $0-25K/yr $25-50K/yr ⱖ$50K/yr
1,217 (74.9) 1,687 (70.4) 1,635 (66.1)
409 (25.2) 711 (29.7) 839 (33.9)
Smoking status Never Former light Former heavy Current light Current heavy
2,182 (69.0) 962 (66.0) 810 (83.4) 122 (74.9) 455 (73.9)
981 (31.0) 495 (34.0) 294 (26.6) 41 (25.2) 161 (26.1)
Diabetes Yes No
650 (69.6) 4,046 (69.7)
284 (30.4) 1,758 (30.3)
⬍ .0001
⬍ .0001
.94
Those with a visible third molar had a significantly greater overall mean PD calculated for all teeth present, except for third molars, compared with those with no visible third molar (P ⬍ .001). The mean PDs were greatest for the visible third molars and incrementally less for the second and first molars and teeth more anterior (Fig 1). The presence of a visible third molar was significantly associated with an increased mean PD on second and first molars compared with the absence of a visible third molar (P ⬍ .0001 and P ⫽ .008, respectively). The mean PDs were lowest on the anterior teeth, canines, and incisors, and no significant differences in the mean PD were found between those with and without a visible third molar. Those with a visible third molar had a significantly greater mean extent of PDs of 4 mm or more calculated from all nonthird molar teeth present compared with those with no visible third molar (8.6% ⫾ 12.4% SD vs 6.8% ⫾ 11.3% SD; P ⬍ .0001, respectively). The mean extent of a PD of 4 mm or more was greatest for the third molars and incrementally less for the teeth more anterior in the mouth, whether a third molar was visible or not. The mean extent of a PD of 4 mm or more at the first and second molars was significantly greater if a third molar had been detected compared with no visible third molar (17.9% ⫾ 19.9% SD vs 15.3% ⫾ 18.6% SD, respectively; P ⬍ .0001; Fig 2, Table 2). The mean extent of a PD of 4 mm or more was low for teeth more anterior in the mouth, less than 10% for premolars and less than 7% for canines and incisors, and not significantly different whether a third molar was visible or not. The results for the mean extent of a PD of 4 mm or more were similar for first and second molars in the model adjusted for covariates. The mean extent of a PD of 4 mm or more for the first and second molars was significantly greater if a third molar had been de-
Data in parentheses are percentages. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
tus. Most had seen a dentist within the previous year (78%) for a regular check-up (73%). Of the 6,793 DARIC participants, 2,035 (30%) had at least 1 visible third molar (Table 1); 970 (14%) had only 1 visible third molar, 490 (7%) had at least 3 visible third molars, and 262 (4%) had 4 third molars. The presence of a visible third molar was significantly associated with black race, male gender, age younger than the mean of 62.4 years, a greater income, never smoking (all P ⬍ .01), and lower education level (P ⫽ .04; Table 1). The presence of a visible third molar was not significantly associated with a diagnosis of diabetes mellitus.
FIGURE 1. Mean periodontal PDs stratified by tooth type. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
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teeth by the presence or absence of a visible third molar, only the mean extent of a CAL of 3 mm or more for the second molars differed significantly (Fig 3B). If only interproximal probing sites were included in the adjusted analyses, the mean extent of a CAL of 3 mm or more was significantly greater for the first and second molars for those with a visible third molar (Fig 3C). However, in both adjusted models, the mean extent of a CAL of 3 mm or more was significantly greater for premolars and for more anterior teeth if no third molar was visible (P ⬍ .01).
Discussion
FIGURE 2. A, Mean percentage of periodontal probing sites with periodontal PDs of at least 4 mm stratified by tooth type. B, Adjusted mean percentage of periodontal probing sites with periodontal PDs of at least 4 mm stratified by tooth type (adjusted for race/center, age, gender, smoking status, education level, and income).
For the middle-age and older participants in the DARIC population, at least 1 visible third molar detected in one third of the subjects was significantly associated with a pattern of the participants having more extensive periodontal disease as assessed by commonly accepted measures including overall mean PD, mean extent (percentage of possible sites) of PD of at least 4 mm, and mean extent (percentage of possible sites) of CAL of at least 3 mm compared with those without a visible third molar. This pattern persisted after controlling for covariates traditionally associated with periodontal disease such as ethnicity/race and smoking. If individual teeth were considered, the data
Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
tected compared with no visible third molar (17.6% ⫾ 0.4% SE vs 15.5% ⫾ 0.3% SE, respectively; P ⬍ .0001; Fig 2A, Table 2). The mean extent of a PD of 4 mm or more for the anterior teeth was significantly greater if a third molar was not visible (P ⫽ .03). The mean extent of a CAL of 3 mm or more at the first and second molars was significantly greater in those with third molar detected compared with those with no visible third molar (20.7% ⫾ 24.6% SD vs 18.4% ⫾ 24.2% SD, respectively; P ⬍ .0006; Fig 3A, Table 3). The mean extent of a CAL of 3 mm or more was less than 11% for the premolars and less than 8% for the more anterior teeth. The mean extent of a CAL of 3 mm or more for the premolars tended to be greater in the presence of a visible third molar (P ⫽ .052). However, the mean extent of a CAL of 3 mm or more was significantly greater for canines and incisors if no third molar was visible (P ⬍ .0001). The results were similar for the combined first and second molars with the adjusted model. The mean extent of a CAL of 3 mm or more was significantly greater if a third molar was visible than if not (20.2% ⫾ 0.5% SE vs 18.6% ⫾ 0.4% SE, respectively; P ⫽ .01; Table 3). However, if the mean extent of a CAL of 3 mm or more were compared for individual
Table 2. UNADJUSTED AND ADJUSTED MEAN EXTENT (PERCENTAGE OF POSSIBLE PROBING SITES) OF PERIODONTAL PROBING DEPTHS OF AT LEAST 4 mm AND STRATIFIED BY THIRD MOLAR PRESENCE
Visible Third Molar Variable
No
Yes
P Value
Unadjusted Anterior teeth 3.35 ⫾ 10.17 3.14 ⫾ 10.02 .44 Premolars 6.70 ⫾ 12.58 6.75 ⫾ 12.75 .88 First and second molars 15.28 ⫾ 18.58 17.94 ⫾ 19.92 ⬍ .0001 Adjusted* Anterior teeth 3.40 ⫾ 0.14 Premolars 6.78 ⫾ 0.18 First and second molars 15.51 ⫾ 0.29
2.82 ⫾ 0.22 6.54 ⫾ 0.28
.03 .47
17.57 ⫾ 0.42
⬍ .0001
Data presented as mean ⫾ SD. Those with visible third molar had significantly greater mean extent of PD of ⱖ4 mm calculated from all remaining teeth present, except for third molars, compared with those with no visible third molar (8.6 ⫾ 12.4 vs 6.8 ⫾ 11.3; P ⬍ .0001, respectively). *Adjusted for race/center, age, gender, smoking status, education level, and income. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
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THIRD MOLARS AND PERIODONTAL PATHOLOGIC FINDINGS
premolars. Also, visible third molars were associated with less severe periodontal disease on the anterior teeth. We could not account for these differences. However, the disease level detected on the anterior teeth by PD or CAL was considerably lower than the disease level detected on the molar teeth, whether visible third molars were present or not. For example, the mean extent of a PD of 4 mm or more for second molars with no visible third molar was 15.8% and for second molars with a visible third molar was 16.8%. The mean extent of a PD of at least 4 mm for central incisors with no visible third molar was 2.6% and for central incisors with a visible third molar was 2.7%. The significant differences we have reported using commonly accepted periodontal measures might seem small to some clinicians. For example, the adjusted mean extent of a PD of at least 4 mm on the second molars was 18.8% for 2,035 subjects with visible third molars compared with 16.0% for the 4,758 subjects with no visible third molars, a significant difference (P ⬍ .01), but a numeric difference of only 2.8%. Similarly, the adjusted interproximal mean CAL of at least 3 mm was 22.1% for those with a visible third molar versus 17.6% for those without a visible third molar, a significant difference (P ⬍ .01), but a numeric difference of only 4.5%. The percentage of differences might appear low, but the differences represent a considerable quantitative difference in disease burden overall for the 2,035 subjects with a visible third molar compared with those without a visible third molar. Hugoson and Kugelberg5 have reported the only data on the prevalence of third molars using both Table 3. UNADJUSTED AND ADJUSTED MEAN EXTENT (PERCENTAGE OF POSSIBLE PROBING SITES) OF CLINICAL ATTACHMENT LEVEL OF AT LEAST 3 mm STRATIFIED BY PRESENCE OF THIRD MOLARS
Visible Third Molars Variable
FIGURE 3. A, Mean percentage of periodontal probing sites with CAL of at least 3 mm stratified by tooth type. B, Adjusted mean percentage of periodontal probing sites with CAL of at least 3 mm stratified by tooth type (adjusted for race/center, age, gender, smoking status, education level, and income). C, Adjusted mean percentage of periodontal probing sites with interproximal CAL of at least 3 mm, stratified by tooth type. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
suggested that the greatest effect of a visible third molar was on the levels of periodontal disease at the first and second molars. These significant periodontal outcomes associated with the presence of third molars did not extend to
Unadjusted Anterior teeth Premolars First and second molars Adjusted* Anterior teeth Premolars First and second molars
No
8.86 ⫾ 19.45 10.43 ⫾ 19.34
Yes
P Value
6.53 ⫾ 15.76 ⬍ .0001 9.51 ⫾ 18.60 .052
18.39 ⫾ 24.17 20.68 ⫾ 24.58
.0006
8.78 ⫾ 0.25 10.47 ⫾ 0.26
6.39 ⫾ 0.39 9.18 ⫾ 0.40
⬍ .0001 .007
18.58 ⫾ 0.36
20.18 ⫾ 0.52
.01
Data presented as mean ⫾ SD. *Adjusted for race/center, age, gender, smoking status, education level, and income. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
MOSS ET AL
clinical and radiographic examinations from subjects representative of an entire population. In their cohort of Swedish subjects, aged 20 years, 98% had at least 1 third molar and 77% had 4 third molars. In each cohort of older subjects, an incrementally greater number of subjects were missing all third molars. No data were reported to substantiate whether third molars were removed because of pathologic features, as a part of other complex treatment, such as orthognathic surgery, or as a preventive measure. Data on the reasons for absent third molars are often missing in population studies and clinical studies. In the Swedish cohort with age comparable to that of the DARIC subjects, 44% of the subjects had at least 1 third molar and 7% had 4 third molars. Moss et al1 reported similar data from the Piedmont 65⫹ study population; 42% had at least 1 visible third molar and 14% had 4 third molars. Fewer DARIC subjects had visible third molars: 30% had at least 1 and 4% had 4 third molars. From these cross-sectional analyses, we could not determine why the DARIC subjects retained fewer third molars nor could we assess what affect having fewer retained third molars might have had on the periodontal outcomes we have reported. Other recent reports from population and clinical studies have also documented an association between the presence of third molars and more severe periodontal disease on more teeth more anterior in the mouth. In 6,000 US subjects, aged 18 to 34 years, in the Third National Health and Nutrition Survey, a visible third molar doubled the odds of finding a PD of at least 5 mm on the adjacent second molar.6 No data on the subjects’ overall level of periodontal disease or the periodontal status of individual teeth more anterior were reported. In a study of 1,000 obstetric subjects enrolled in the Oral Conditions and Pregnancy study, those with a visible third molar were significantly more likely to have moderate to severe periodontal disease and less likely to be periodontally healthy at enrollment during the second trimester and at postpartum examinations.7 In the same obstetric subjects, between the second trimester and the postpartum examination, periodontal progression (4 or more probing sites with an at least 2-mm increase in PD, all at least 4 mm in depth) was greater if at least 1 PD of 4 mm or more or bleeding on probing had been detected at the third molars at enrollment.8 Similar to the DARIC subjects, periodontal disease detected in the obstetric subjects was more likely in the molar regions of the mouth, at interproximal molar probing sites, and most likely around the third molars. Is it plausible that periodontal inflammatory disease would be detected more often on the first and second molars when third molars are present? Our previous work has suggested that the anatomic location of
2597 third molars makes these teeth more conducive to the colonization of pathogens, more likely to have at least 1 PD of 4 mm or more, and less amenable to mechanical debridement targeted to altering pathogen levels.9-12 One quarter of young adults with 4 asymptomatic third molars enrolled in a longitudinal study designed to follow up subjects with 4 asymptomatic third molars over time had at least 1 periodontal PD of 5 mm or more in the third molar region at the baseline examination, defined as 2 probing sites on the distal of the second molars and 6 probing sites around the third molars.10 Two thirds of the subjects had at least 1 PD of 4 mm or more in the third molar region; only one third of the same subjects had a PD of 4 mm or more on the periodontal probing sites of teeth anterior to the second molars.11 With time, third molar periodontal disease was associated with periodontal disease at the teeth more anterior. At 6 years after enrollment, the periodontal pathologic findings had worsened for the third molar region and nonthird molars.11 The presence of at least 1 third molar region with a PD of 4 mm or more at the baseline examination increased the risk 12-fold of at least 4 PDs greater than 4 mm being detected in the third molar region.12 The presence of at least 1 third molar region with a PD of 4 mm or more at the baseline examination increased the risk almost fourfold of periodontal pathologic findings at the nonthird molar teeth 6 years later compared with those with a PD of less than 4 mm in the third molar region at enrollment.12 Does a biologic basis exist to explain the association between the presence of third molars and periodontal disease at the first and second molars? In those affected, the clinical signs (PD of 4 mm or more and bleeding on probing) result from the interaction of periodontal pathogens with the immune system at the biofilm gingival interface.13 Once teeth have been exposed to the oral cavity and can be probed, oral flora colonize on the surfaces in a nonsheddable biofilm. Pathogens colonized in this nonsheddable biofilm interface with an adjacent single epithelial layer with underlying immune system cells (neutrophils, lymphocytes, and monocytes) and abundant underlying vascular tissue. The magnitude and quality of the local host inflammatory response to the presence of bacteria in the biofilm are reflected in the local production of gingival crevicular fluid inflammatory mediators, chiefly from immune system cells. Clinically, the collective PDs at 6 sites per tooth offer an estimate of the total surface area of the biofilm gingival interface. As the total surface area increases, reflected by increasing numbers of deeper PDs, the more the anaerobic environment facilitates colonization of pathogens, increasing the potential for the host to have more severe periodontal inflammatory disease.12,13
2598 PDs of at least 4 mm have been detected more often around mandibular third molars than other exposed teeth.14 Third molars are the most posterior teeth in each jaw, erupting last, on average at age 19.4 years.15 Mandibular third molars are situated anatomically in the alveolar bone at the junction of the horizontal body of the jaw and the vertical ramus. The combined effect of erupting at a later age than the other teeth and the anatomic location in the jaw might be the reason for the greater prevalence of PDs of 4 mm or more found around mandibular third molars. Once established, bacteria around the third molars are difficult to eradicate with mechanical debridement alone, and pathogens in third molar sites might serve as a potential reservoir for pathogens colonizing other sites.9 How should clinicians apply these findings from the population data to their individual patients? The topic of retained third molars and an association with periodontal disease in young and older adults has only been studied in the past decade. We report a pattern of a significant association between visible third molars and periodontal inflammatory disease. These data do not suggest a cause and effect. However, the collective data from subjects in the DARIC study, Third National Health and Nutrition Survey, and Oral Conditions and Pregnancy study suggest that more extensive periodontal disease might be detected in the molar regions of the mouth when third molars are present. These findings implying that retained third molars are not always benign are not appreciated well by the public and might not be evident to some dentists or physicians. Additional investigations are needed on this topic; however, a retained third molar alone might be a risk marker alerting clinicians to the possibility of an increased risk of periodontal pathologic findings affecting teeth more anterior in the mouth, particularly the first and second molars. The findings we report from the DARIC study have limits and might not be applicable to all middle-age and older subjects. Although our study population numbered almost 7,000, only 4 communities in the United States were represented. The participants in the DARIC study were enrolled for a study of cardiovascular disease, not periodontal inflammatory disease. If a representative sample of all subjects of a similar age in the United States were studied, covariates such as socioeconomic level, health status, smoking status, and ethnicity might or might not be as significantly associated with periodontal pathologic findings as retained third molars. The number of third molars in the DARIC participants might have been understated because radiographs to detect impacted teeth were not available to the examiners. Few population studies have reported on the reasons the third
THIRD MOLARS AND PERIODONTAL PATHOLOGIC FINDINGS
molars were absent, including the data from the DARIC study. Thus, we do not know whether the missing third molars were removed to treat existing disease or to prevent future pathologic features. Therefore, our data on periodontal pathologic features with retained third molars might have been under- or overstated. However, our data do suggest that the pattern of the association between third molars and periodontal pathologic features on teeth more anterior in the mouth should be studied further in other populations. Acknowledgment We thank the staff and participants of the Atherosclerosis Risk in Communities study for their important contributions. The present report was reviewed and approved by the Atherosclerosis Risk in Communities Coordinating Committee.
References 1. Elter JR, Offenbacher S, White RP Jr: Third molars associated with periodontal pathology in older Americans. J Oral Maxillofac Surg 63:179, 2005 2. Moss KL, Beck JD, Mauriello SM, et al: Third molar periodontal pathology and caries in senior adults. J Oral Maxillofac Surg 65:103, 2007 3. Atherosclerosis Risk in Communities Investigators: The Atherosclerosis Risk in Communities (ARIC) study: Design objectives. Am J Epidemiol 129:687, 1989 4. Beck JD, Elter JR, Heiss G, et al: Relationship of periodontal disease to carotid artery intima-media wall thickness: The Atherosclerosis Risk in Communities (ARIC) study. Arterioscler Thromb Vasc Biol 21:1816, 2001 5. Hugoson A, Kugelberg CF: The prevalence of third molars in a Swedish population: An epidemiological study. Commun Dent Health 5:121, 1988 6. Elter JR, Cuomo C, Slade GD, et al: Third molars associated with periodontal pathology in the third national health and nutrition examination survey. J Oral Maxillofac Surg 62:440, 2004 7. Moss KL, Serlo AD, Offenbacher S, et al: The oral and systemic impact of third molar periodontal pathology. J Oral Maxillofac Surg 65:1739, 2007 8. Moss KL, Ruvo AT, Offenbacher S, et al: Third molars and progression of periodontal pathology during pregnancy. J Oral Maxillofac Surg 65:1065, 2007 9. Moss KL, Serlo AD, Offenbacher S, et al: Third molars and the efficacy of mechanical debridement in reducing pathogen levels in pregnant subjects: A pilot study. J Oral Maxillofac Surg 66:1565, 2008 10. Blakey GH, Marciani RD, Haug RH, et al: Periodontal pathology associated with asymptomatic third molars. J Oral Maxillofac Surg 60:1227, 2002 11. Blakey GH, Hull D, Haug RH, et al: Changes in third molar and non-third molar periodontal pathology over time. J Oral Maxillofac Surg 65:1577, 2007 12. White RP Jr, Phillips C, Hull DJ, et al: Risk markers for progression of periodontal pathology in the third molar and non-third molar regions in young adults. J Oral Maxillofac Surg 66:749, 2008 13. Offenbacher S, Barros SP, Singer RE, et al: Periodontal disease at the biofilm-gingival interface. J Periodontol 78:1911, 2007 14. Blakey GH, Jacks MT, Offenbacher S, et al: Progression of periodontal disease in the second/third molar region in patients with asymptomatic third molars. J Oral Maxillofac Surg 64:189, 2006 15. Rantanen AV: The age of eruption of the third molar teeth. Acta Odontol Scand 25:48, 1967 (suppl 1)
Third Molars and Periodontal Pathologic Findings in Middle-Age and Older Americans Kevin L. Moss,* Esther S. Oh, DDS, MD,† Elda Fisher, DMD,‡ James D. Beck, PhD,§ Steven Offenbacher, DDS, PhD,¶ and Raymond P. White, Jr, DDS, PhD储 Purpose: To assess the association between the visible presence of third molars and the severity of
periodontal pathologic findings on teeth more anterior in the mouth. Patients and Methods: The present analysis included dentate participants, 52 to 74 years old, from the
Dental Atherosclerosis Risk in Communities study who had undergone an oral examination that included periodontal probing depths (PDs) on all visible teeth, including any third molars. A PD of 4 mm or more and a clinical attachment level of 3 mm or greater were indicator variables for periodontal pathologic features. Explanatory variables were the presence or absence of visible third molars. The covariates included gender, ethnicity, age, income level, education, and smoking status. The outcome variables for periodontal pathologic features were the mean PD, extent (percentage of probing sites) of PDs of 4 mm or more, and the extent (percentage of probing sites) of a clinical attachment level of 3 mm or more. The outcomes between those with and without visible third molars were compared using descriptive statistics and chi-square tests, with significance set at P ⫽ .05. Multivariate modeling was performed using Statistical Analysis Systems SAS Proc GLM (SAS Institute, Cary, NC) to calculate the least squared means, adjusting for the study outcome variables and covariates. Results: The Dental Atherosclerosis Risk in Communities study sample included 6,793 subjects; 80% were white and 19% were black. Most (53%) were 62 to 74 years old and female (54%). Of the 6,793 participants, 2,035 (30%) had at least 1 visible third molar. The presence of a visible third molar was significantly associated with male gender, black race, age younger than the mean of 62.4 years, greater income, and never smoking (all P ⬍ .01). A greater mean PD for the first and second molars, the extent of PD of 4 mm or more at the first and second molars, and the extent of a clinical attachment level of 3 mm or more at the first and second molars were all significantly associated with the presence of a visible third molar in the unadjusted and adjusted models. Conclusions: In these middle-age and older Americans, the presence of a visible third molar was significantly associated with more severe periodontal disease on teeth more anterior in the mouth compared with those subjects with no visible third molars. © 2009 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 67:2592-2598, 2009
Received from the University of North Carolina School of Dentistry, Chapel Hill, NC. *Research Specialist, Department of Dental Ecology. †Resident, Department of Oral and Maxillofacial Surgery. ‡Resident, Department of Oral and Maxillofacial Surgery. §Kenan Distinguished Professor, Associate Dean for Research, Department of Dental Ecology. ¶OraPharma Distinguished Professor, Department of Periodontology. 储Dalton L. McMichael Distinguished Professor, Department of Oral and Maxillofacial Surgery. The Atherosclerosis Risk in Communities Study was performed as a collaborative study supported by National Heart,
Lung, and Blood Institute grants N01-HC-55015, N01-HC-55016, N01-HC-55018, N01-HC-55019, N01-HC-55020, N01-HC-55021, and N01-HC-55022. The present analyses were supported by National Institute of Dental and Craniofacial Research grant R01DE 11551. Grant support provided by the OMS Foundation, AAOMS. Address correspondence and reprint requests to Dr White: Department of Oral and Maxillofacial Surgery, University of North Carolina School of Dentistry, CB 7450, Chapel Hill, NC 27559-7450; e-mail: [email protected] © 2009 American Association of Oral and Maxillofacial Surgeons
0278-2391/09/6712-0007$36.00/0 doi:10.1016/j.joms.2009.04.046
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Clinicians are hampered in providing advice to their patients about the management of third molars because few population data exist from the United States on the presence or absence of third molars, and third molars are often not included in clinical studies of periodontal inflammatory disease. Elter et al1 reported a significant association between identifying a visible third molar and the periodontal health of an adjacent second molar in the dentate subjects with an average age of 62 years from the Dental Atherosclerosis Risk in Communities (DARIC) study. A visible third molar was associated with 1.5 times the odds of detecting at least 1 periodontal probing depth (PD) of 5 mm or more or bleeding on probing of the adjacent second molar, controlling for other factors associated with the visible presence of third molars and periodontal disease. Their report did not assess periodontal disease affecting third molars nor the severity of periodontal disease of DARIC subjects on teeth anterior to the second molars. From an older population in North Carolina with an average age of 73 years, Moss et al2 reported that 42% of dentate subjects had at least 1 third molar and 14% subjects had 4 third molars. Periodontal disease was not exclusive to the third molars in this population of senior adults. If teeth more anterior to third molars were not affected, fewer than 1% subjects had at least 1 third molar clinical attachment level (CAL) of 3 mm or more, and only 8% of subjects had at least 1 third molar PD of 4 mm or more. The relationship between the visible presence of third molars versus no visible third molars and patients’ periodontal disease level was not reported. The present study was designed to further our understanding of the association between retained third molars and periodontal inflammatory disease by studying the population of DARIC subjects to document the presence or absence of visible third molars and assess the association between the visible presence of third molars and the severity of periodontal pathologic findings on teeth more anterior than third molars using commonly applied measures of periodontal inflammatory disease, including the mean PD, extent (percentage of sites) of PD of 4 mm or more, and extent (percentage of sites) of CAL of 3 mm or more.
sites, with data collected from 1996 to 1998. The cross-sectional study included all dentate Atherosclerosis Risk in Communities participants aged 52 to 74 years who had undergone a periodontal examination. Those with a medical contraindication to periodontal probing were excluded. The DARIC oral examination was conducted by trained, calibrated examiners and included the periodontal PDs, 6 sites per tooth, for all visible teeth, including the third molars. No radiographs were available to complement the clinical examinations. Additional details of the DARIC study are provided in the report by Beck et al.4 The participants’ mean PD, PD of 4 mm or more, and CAL of 3 mm or more at the third molars and more anterior teeth were considered indicator variables for periodontal pathologic features. For our analyses, the DARIC participants were divided into 2 groups according to the presence of at least 1 visible third molar versus no visible third molar, main explanatory variables. Covariates included gender, ethnicity/race (black or white), age, income level per year (less than $25K, $25 to 50K, and more than $50K), level of education (basic [less than high school], intermediate [high school graduate], and advanced [more than high school]), and smoking status (current, former, or never). The outcome variables for the subjects’ level of periodontal pathologic disease were the mean periodontal PD, the mean extent (percentage of probing sites) with a PD of 4 mm or more, and the mean extent (percentage of probing sites) with a CAL of 3 mm or more. The outcomes between those with and without a visible third molar were compared using descriptive statistics and chi-square or t tests, with statistical significance set at P ⫽ .05. The potential confounders of ethnicity by study center, gender, smoking, age, education, and income were added to the adjusted models according to their association with the visible presence or absence of a third molar. Multivariable modeling was performed using Statistical Analysis Systems SAS Proc GLM (SAS Institute, Cary, NC) to calculate the least squared means, adjusting for outcome variables and covariates.
Results Patients and Methods The DARIC study, an institutional review board-approved substudy of the Atherosclerosis Risk in Communities Study, targeted 4 sites in the United States: Forsyth County, North Carolina; Jackson, Mississippi; suburbs of Minneapolis, Minnesota; and Washington County, Maryland.3 The oral examination involved participants at the Atherosclerosis Risk in Communities’ 4
The mean age of the 6,793 DARIC participants was 62.4 ⫾ 5.6 years. More of the participants were women (54%); 80% were white and 19% were black. Of the 6,793 participants, 86% had at least a high school education and 43% had been educated beyond high school. More than one half of the subjects were current (12%) or former (39%) smokers, and 14% of all participants had been diagnosed with diabetes melli-
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Table 1. CHARACTERISTICS OF DENTAL ATHEROSCLEROSIS RISK IN COMMUNITIES’ PARTICIPANTS (n ⴝ 6,793; 4,758 HAD NO VISIBLE THIRD MOLARS, 2,035 HAD AT LEAST 1 VISIBLE THIRD MOLAR)
Third Molar Visible Characteristic
No
Yes
Race Black White
819 (65.0) 3,865 (70.9)
441 (35.0) 1,588 (29.1)
Gender Female Male
2,764 (75.6) 1,932 (62.7)
894 (24.4) 1,148 (37.3)
Mean age (yr)
62.8 ⫾ 5.66
61.6 ⫾ 5.47
Education level Less than high school (0-ⱕ11 yr) High school graduate (12-16 yr) More than high school (ⱖ17 yr)
P Value ⬍ .0001
⬍ .0001
⬍ .0001 .04
662 (73.1)
244 (26.9)
2,023 (69.8)
877 (30.2)
2,005 (68.6)
918 (31.4)
Income $0-25K/yr $25-50K/yr ⱖ$50K/yr
1,217 (74.9) 1,687 (70.4) 1,635 (66.1)
409 (25.2) 711 (29.7) 839 (33.9)
Smoking status Never Former light Former heavy Current light Current heavy
2,182 (69.0) 962 (66.0) 810 (83.4) 122 (74.9) 455 (73.9)
981 (31.0) 495 (34.0) 294 (26.6) 41 (25.2) 161 (26.1)
Diabetes Yes No
650 (69.6) 4,046 (69.7)
284 (30.4) 1,758 (30.3)
⬍ .0001
⬍ .0001
.94
Those with a visible third molar had a significantly greater overall mean PD calculated for all teeth present, except for third molars, compared with those with no visible third molar (P ⬍ .001). The mean PDs were greatest for the visible third molars and incrementally less for the second and first molars and teeth more anterior (Fig 1). The presence of a visible third molar was significantly associated with an increased mean PD on second and first molars compared with the absence of a visible third molar (P ⬍ .0001 and P ⫽ .008, respectively). The mean PDs were lowest on the anterior teeth, canines, and incisors, and no significant differences in the mean PD were found between those with and without a visible third molar. Those with a visible third molar had a significantly greater mean extent of PDs of 4 mm or more calculated from all nonthird molar teeth present compared with those with no visible third molar (8.6% ⫾ 12.4% SD vs 6.8% ⫾ 11.3% SD; P ⬍ .0001, respectively). The mean extent of a PD of 4 mm or more was greatest for the third molars and incrementally less for the teeth more anterior in the mouth, whether a third molar was visible or not. The mean extent of a PD of 4 mm or more at the first and second molars was significantly greater if a third molar had been detected compared with no visible third molar (17.9% ⫾ 19.9% SD vs 15.3% ⫾ 18.6% SD, respectively; P ⬍ .0001; Fig 2, Table 2). The mean extent of a PD of 4 mm or more was low for teeth more anterior in the mouth, less than 10% for premolars and less than 7% for canines and incisors, and not significantly different whether a third molar was visible or not. The results for the mean extent of a PD of 4 mm or more were similar for first and second molars in the model adjusted for covariates. The mean extent of a PD of 4 mm or more for the first and second molars was significantly greater if a third molar had been de-
Data in parentheses are percentages. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
tus. Most had seen a dentist within the previous year (78%) for a regular check-up (73%). Of the 6,793 DARIC participants, 2,035 (30%) had at least 1 visible third molar (Table 1); 970 (14%) had only 1 visible third molar, 490 (7%) had at least 3 visible third molars, and 262 (4%) had 4 third molars. The presence of a visible third molar was significantly associated with black race, male gender, age younger than the mean of 62.4 years, a greater income, never smoking (all P ⬍ .01), and lower education level (P ⫽ .04; Table 1). The presence of a visible third molar was not significantly associated with a diagnosis of diabetes mellitus.
FIGURE 1. Mean periodontal PDs stratified by tooth type. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
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teeth by the presence or absence of a visible third molar, only the mean extent of a CAL of 3 mm or more for the second molars differed significantly (Fig 3B). If only interproximal probing sites were included in the adjusted analyses, the mean extent of a CAL of 3 mm or more was significantly greater for the first and second molars for those with a visible third molar (Fig 3C). However, in both adjusted models, the mean extent of a CAL of 3 mm or more was significantly greater for premolars and for more anterior teeth if no third molar was visible (P ⬍ .01).
Discussion
FIGURE 2. A, Mean percentage of periodontal probing sites with periodontal PDs of at least 4 mm stratified by tooth type. B, Adjusted mean percentage of periodontal probing sites with periodontal PDs of at least 4 mm stratified by tooth type (adjusted for race/center, age, gender, smoking status, education level, and income).
For the middle-age and older participants in the DARIC population, at least 1 visible third molar detected in one third of the subjects was significantly associated with a pattern of the participants having more extensive periodontal disease as assessed by commonly accepted measures including overall mean PD, mean extent (percentage of possible sites) of PD of at least 4 mm, and mean extent (percentage of possible sites) of CAL of at least 3 mm compared with those without a visible third molar. This pattern persisted after controlling for covariates traditionally associated with periodontal disease such as ethnicity/race and smoking. If individual teeth were considered, the data
Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
tected compared with no visible third molar (17.6% ⫾ 0.4% SE vs 15.5% ⫾ 0.3% SE, respectively; P ⬍ .0001; Fig 2A, Table 2). The mean extent of a PD of 4 mm or more for the anterior teeth was significantly greater if a third molar was not visible (P ⫽ .03). The mean extent of a CAL of 3 mm or more at the first and second molars was significantly greater in those with third molar detected compared with those with no visible third molar (20.7% ⫾ 24.6% SD vs 18.4% ⫾ 24.2% SD, respectively; P ⬍ .0006; Fig 3A, Table 3). The mean extent of a CAL of 3 mm or more was less than 11% for the premolars and less than 8% for the more anterior teeth. The mean extent of a CAL of 3 mm or more for the premolars tended to be greater in the presence of a visible third molar (P ⫽ .052). However, the mean extent of a CAL of 3 mm or more was significantly greater for canines and incisors if no third molar was visible (P ⬍ .0001). The results were similar for the combined first and second molars with the adjusted model. The mean extent of a CAL of 3 mm or more was significantly greater if a third molar was visible than if not (20.2% ⫾ 0.5% SE vs 18.6% ⫾ 0.4% SE, respectively; P ⫽ .01; Table 3). However, if the mean extent of a CAL of 3 mm or more were compared for individual
Table 2. UNADJUSTED AND ADJUSTED MEAN EXTENT (PERCENTAGE OF POSSIBLE PROBING SITES) OF PERIODONTAL PROBING DEPTHS OF AT LEAST 4 mm AND STRATIFIED BY THIRD MOLAR PRESENCE
Visible Third Molar Variable
No
Yes
P Value
Unadjusted Anterior teeth 3.35 ⫾ 10.17 3.14 ⫾ 10.02 .44 Premolars 6.70 ⫾ 12.58 6.75 ⫾ 12.75 .88 First and second molars 15.28 ⫾ 18.58 17.94 ⫾ 19.92 ⬍ .0001 Adjusted* Anterior teeth 3.40 ⫾ 0.14 Premolars 6.78 ⫾ 0.18 First and second molars 15.51 ⫾ 0.29
2.82 ⫾ 0.22 6.54 ⫾ 0.28
.03 .47
17.57 ⫾ 0.42
⬍ .0001
Data presented as mean ⫾ SD. Those with visible third molar had significantly greater mean extent of PD of ⱖ4 mm calculated from all remaining teeth present, except for third molars, compared with those with no visible third molar (8.6 ⫾ 12.4 vs 6.8 ⫾ 11.3; P ⬍ .0001, respectively). *Adjusted for race/center, age, gender, smoking status, education level, and income. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
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THIRD MOLARS AND PERIODONTAL PATHOLOGIC FINDINGS
premolars. Also, visible third molars were associated with less severe periodontal disease on the anterior teeth. We could not account for these differences. However, the disease level detected on the anterior teeth by PD or CAL was considerably lower than the disease level detected on the molar teeth, whether visible third molars were present or not. For example, the mean extent of a PD of 4 mm or more for second molars with no visible third molar was 15.8% and for second molars with a visible third molar was 16.8%. The mean extent of a PD of at least 4 mm for central incisors with no visible third molar was 2.6% and for central incisors with a visible third molar was 2.7%. The significant differences we have reported using commonly accepted periodontal measures might seem small to some clinicians. For example, the adjusted mean extent of a PD of at least 4 mm on the second molars was 18.8% for 2,035 subjects with visible third molars compared with 16.0% for the 4,758 subjects with no visible third molars, a significant difference (P ⬍ .01), but a numeric difference of only 2.8%. Similarly, the adjusted interproximal mean CAL of at least 3 mm was 22.1% for those with a visible third molar versus 17.6% for those without a visible third molar, a significant difference (P ⬍ .01), but a numeric difference of only 4.5%. The percentage of differences might appear low, but the differences represent a considerable quantitative difference in disease burden overall for the 2,035 subjects with a visible third molar compared with those without a visible third molar. Hugoson and Kugelberg5 have reported the only data on the prevalence of third molars using both Table 3. UNADJUSTED AND ADJUSTED MEAN EXTENT (PERCENTAGE OF POSSIBLE PROBING SITES) OF CLINICAL ATTACHMENT LEVEL OF AT LEAST 3 mm STRATIFIED BY PRESENCE OF THIRD MOLARS
Visible Third Molars Variable
FIGURE 3. A, Mean percentage of periodontal probing sites with CAL of at least 3 mm stratified by tooth type. B, Adjusted mean percentage of periodontal probing sites with CAL of at least 3 mm stratified by tooth type (adjusted for race/center, age, gender, smoking status, education level, and income). C, Adjusted mean percentage of periodontal probing sites with interproximal CAL of at least 3 mm, stratified by tooth type. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
suggested that the greatest effect of a visible third molar was on the levels of periodontal disease at the first and second molars. These significant periodontal outcomes associated with the presence of third molars did not extend to
Unadjusted Anterior teeth Premolars First and second molars Adjusted* Anterior teeth Premolars First and second molars
No
8.86 ⫾ 19.45 10.43 ⫾ 19.34
Yes
P Value
6.53 ⫾ 15.76 ⬍ .0001 9.51 ⫾ 18.60 .052
18.39 ⫾ 24.17 20.68 ⫾ 24.58
.0006
8.78 ⫾ 0.25 10.47 ⫾ 0.26
6.39 ⫾ 0.39 9.18 ⫾ 0.40
⬍ .0001 .007
18.58 ⫾ 0.36
20.18 ⫾ 0.52
.01
Data presented as mean ⫾ SD. *Adjusted for race/center, age, gender, smoking status, education level, and income. Moss et al. Third Molars and Periodontal Pathologic Findings. J Oral Maxillofac Surg 2009.
MOSS ET AL
clinical and radiographic examinations from subjects representative of an entire population. In their cohort of Swedish subjects, aged 20 years, 98% had at least 1 third molar and 77% had 4 third molars. In each cohort of older subjects, an incrementally greater number of subjects were missing all third molars. No data were reported to substantiate whether third molars were removed because of pathologic features, as a part of other complex treatment, such as orthognathic surgery, or as a preventive measure. Data on the reasons for absent third molars are often missing in population studies and clinical studies. In the Swedish cohort with age comparable to that of the DARIC subjects, 44% of the subjects had at least 1 third molar and 7% had 4 third molars. Moss et al1 reported similar data from the Piedmont 65⫹ study population; 42% had at least 1 visible third molar and 14% had 4 third molars. Fewer DARIC subjects had visible third molars: 30% had at least 1 and 4% had 4 third molars. From these cross-sectional analyses, we could not determine why the DARIC subjects retained fewer third molars nor could we assess what affect having fewer retained third molars might have had on the periodontal outcomes we have reported. Other recent reports from population and clinical studies have also documented an association between the presence of third molars and more severe periodontal disease on more teeth more anterior in the mouth. In 6,000 US subjects, aged 18 to 34 years, in the Third National Health and Nutrition Survey, a visible third molar doubled the odds of finding a PD of at least 5 mm on the adjacent second molar.6 No data on the subjects’ overall level of periodontal disease or the periodontal status of individual teeth more anterior were reported. In a study of 1,000 obstetric subjects enrolled in the Oral Conditions and Pregnancy study, those with a visible third molar were significantly more likely to have moderate to severe periodontal disease and less likely to be periodontally healthy at enrollment during the second trimester and at postpartum examinations.7 In the same obstetric subjects, between the second trimester and the postpartum examination, periodontal progression (4 or more probing sites with an at least 2-mm increase in PD, all at least 4 mm in depth) was greater if at least 1 PD of 4 mm or more or bleeding on probing had been detected at the third molars at enrollment.8 Similar to the DARIC subjects, periodontal disease detected in the obstetric subjects was more likely in the molar regions of the mouth, at interproximal molar probing sites, and most likely around the third molars. Is it plausible that periodontal inflammatory disease would be detected more often on the first and second molars when third molars are present? Our previous work has suggested that the anatomic location of
2597 third molars makes these teeth more conducive to the colonization of pathogens, more likely to have at least 1 PD of 4 mm or more, and less amenable to mechanical debridement targeted to altering pathogen levels.9-12 One quarter of young adults with 4 asymptomatic third molars enrolled in a longitudinal study designed to follow up subjects with 4 asymptomatic third molars over time had at least 1 periodontal PD of 5 mm or more in the third molar region at the baseline examination, defined as 2 probing sites on the distal of the second molars and 6 probing sites around the third molars.10 Two thirds of the subjects had at least 1 PD of 4 mm or more in the third molar region; only one third of the same subjects had a PD of 4 mm or more on the periodontal probing sites of teeth anterior to the second molars.11 With time, third molar periodontal disease was associated with periodontal disease at the teeth more anterior. At 6 years after enrollment, the periodontal pathologic findings had worsened for the third molar region and nonthird molars.11 The presence of at least 1 third molar region with a PD of 4 mm or more at the baseline examination increased the risk 12-fold of at least 4 PDs greater than 4 mm being detected in the third molar region.12 The presence of at least 1 third molar region with a PD of 4 mm or more at the baseline examination increased the risk almost fourfold of periodontal pathologic findings at the nonthird molar teeth 6 years later compared with those with a PD of less than 4 mm in the third molar region at enrollment.12 Does a biologic basis exist to explain the association between the presence of third molars and periodontal disease at the first and second molars? In those affected, the clinical signs (PD of 4 mm or more and bleeding on probing) result from the interaction of periodontal pathogens with the immune system at the biofilm gingival interface.13 Once teeth have been exposed to the oral cavity and can be probed, oral flora colonize on the surfaces in a nonsheddable biofilm. Pathogens colonized in this nonsheddable biofilm interface with an adjacent single epithelial layer with underlying immune system cells (neutrophils, lymphocytes, and monocytes) and abundant underlying vascular tissue. The magnitude and quality of the local host inflammatory response to the presence of bacteria in the biofilm are reflected in the local production of gingival crevicular fluid inflammatory mediators, chiefly from immune system cells. Clinically, the collective PDs at 6 sites per tooth offer an estimate of the total surface area of the biofilm gingival interface. As the total surface area increases, reflected by increasing numbers of deeper PDs, the more the anaerobic environment facilitates colonization of pathogens, increasing the potential for the host to have more severe periodontal inflammatory disease.12,13
2598 PDs of at least 4 mm have been detected more often around mandibular third molars than other exposed teeth.14 Third molars are the most posterior teeth in each jaw, erupting last, on average at age 19.4 years.15 Mandibular third molars are situated anatomically in the alveolar bone at the junction of the horizontal body of the jaw and the vertical ramus. The combined effect of erupting at a later age than the other teeth and the anatomic location in the jaw might be the reason for the greater prevalence of PDs of 4 mm or more found around mandibular third molars. Once established, bacteria around the third molars are difficult to eradicate with mechanical debridement alone, and pathogens in third molar sites might serve as a potential reservoir for pathogens colonizing other sites.9 How should clinicians apply these findings from the population data to their individual patients? The topic of retained third molars and an association with periodontal disease in young and older adults has only been studied in the past decade. We report a pattern of a significant association between visible third molars and periodontal inflammatory disease. These data do not suggest a cause and effect. However, the collective data from subjects in the DARIC study, Third National Health and Nutrition Survey, and Oral Conditions and Pregnancy study suggest that more extensive periodontal disease might be detected in the molar regions of the mouth when third molars are present. These findings implying that retained third molars are not always benign are not appreciated well by the public and might not be evident to some dentists or physicians. Additional investigations are needed on this topic; however, a retained third molar alone might be a risk marker alerting clinicians to the possibility of an increased risk of periodontal pathologic findings affecting teeth more anterior in the mouth, particularly the first and second molars. The findings we report from the DARIC study have limits and might not be applicable to all middle-age and older subjects. Although our study population numbered almost 7,000, only 4 communities in the United States were represented. The participants in the DARIC study were enrolled for a study of cardiovascular disease, not periodontal inflammatory disease. If a representative sample of all subjects of a similar age in the United States were studied, covariates such as socioeconomic level, health status, smoking status, and ethnicity might or might not be as significantly associated with periodontal pathologic findings as retained third molars. The number of third molars in the DARIC participants might have been understated because radiographs to detect impacted teeth were not available to the examiners. Few population studies have reported on the reasons the third
THIRD MOLARS AND PERIODONTAL PATHOLOGIC FINDINGS
molars were absent, including the data from the DARIC study. Thus, we do not know whether the missing third molars were removed to treat existing disease or to prevent future pathologic features. Therefore, our data on periodontal pathologic features with retained third molars might have been under- or overstated. However, our data do suggest that the pattern of the association between third molars and periodontal pathologic features on teeth more anterior in the mouth should be studied further in other populations. Acknowledgment We thank the staff and participants of the Atherosclerosis Risk in Communities study for their important contributions. The present report was reviewed and approved by the Atherosclerosis Risk in Communities Coordinating Committee.
References 1. Elter JR, Offenbacher S, White RP Jr: Third molars associated with periodontal pathology in older Americans. J Oral Maxillofac Surg 63:179, 2005 2. Moss KL, Beck JD, Mauriello SM, et al: Third molar periodontal pathology and caries in senior adults. J Oral Maxillofac Surg 65:103, 2007 3. Atherosclerosis Risk in Communities Investigators: The Atherosclerosis Risk in Communities (ARIC) study: Design objectives. Am J Epidemiol 129:687, 1989 4. Beck JD, Elter JR, Heiss G, et al: Relationship of periodontal disease to carotid artery intima-media wall thickness: The Atherosclerosis Risk in Communities (ARIC) study. Arterioscler Thromb Vasc Biol 21:1816, 2001 5. Hugoson A, Kugelberg CF: The prevalence of third molars in a Swedish population: An epidemiological study. Commun Dent Health 5:121, 1988 6. Elter JR, Cuomo C, Slade GD, et al: Third molars associated with periodontal pathology in the third national health and nutrition examination survey. J Oral Maxillofac Surg 62:440, 2004 7. Moss KL, Serlo AD, Offenbacher S, et al: The oral and systemic impact of third molar periodontal pathology. J Oral Maxillofac Surg 65:1739, 2007 8. Moss KL, Ruvo AT, Offenbacher S, et al: Third molars and progression of periodontal pathology during pregnancy. J Oral Maxillofac Surg 65:1065, 2007 9. Moss KL, Serlo AD, Offenbacher S, et al: Third molars and the efficacy of mechanical debridement in reducing pathogen levels in pregnant subjects: A pilot study. J Oral Maxillofac Surg 66:1565, 2008 10. Blakey GH, Marciani RD, Haug RH, et al: Periodontal pathology associated with asymptomatic third molars. J Oral Maxillofac Surg 60:1227, 2002 11. Blakey GH, Hull D, Haug RH, et al: Changes in third molar and non-third molar periodontal pathology over time. J Oral Maxillofac Surg 65:1577, 2007 12. White RP Jr, Phillips C, Hull DJ, et al: Risk markers for progression of periodontal pathology in the third molar and non-third molar regions in young adults. J Oral Maxillofac Surg 66:749, 2008 13. Offenbacher S, Barros SP, Singer RE, et al: Periodontal disease at the biofilm-gingival interface. J Periodontol 78:1911, 2007 14. Blakey GH, Jacks MT, Offenbacher S, et al: Progression of periodontal disease in the second/third molar region in patients with asymptomatic third molars. J Oral Maxillofac Surg 64:189, 2006 15. Rantanen AV: The age of eruption of the third molar teeth. Acta Odontol Scand 25:48, 1967 (suppl 1)