- Email: [email protected]
Caries Experience and Periodontal Pathology in Erupting Third Molars
J Oral Maxillofac Surg 66:948-953, 2008
Caries Experience and Periodontal Pathology in Erupting Third Molars Nazir Ahmad,* Savannah Gelesko,† Daniel Shugars, DDS, PhD, MPH,‡ Raymond P. White, Jr, DDS, PhD,§ George Blakey, DDS,储 Richard H. Haug, DDS,¶ Steven Offenbacher, DDS, PhD,** and Ceib Phillips, PhD, MPH†† Purpose: This study was conducted to document the prevalence of occlusal caries experience and
periodontal pathology for erupting third molars in young adults. Patients and Methods: The data are from 49 subjects enrolled in an institutional review board–approved trial with at least one third molar below the occlusal plane at baseline that erupted by longest follow-up. Teeth were considered erupted if they reached the occlusal plane. Caries experience on the occlusal surface of third molars was assessed by a visual-tactile examination. At least 1 periodontal probing depth (PD) ⱖ4 mm in the third molar region was considered indicative of periodontal pathology. The third molar region was defined as the 6 probing sites around third molars and 2 sites on the distal of second molars. The prevalence of third molar caries experience and periodontal pathology at longest follow-up was assessed. Results: Most of the 49 subjects were female (51%), Caucasian (76%), and educated at least through high school (82%). Median age was 20.5 years (interquartile range [IQR] 18.4 to 24.1 years). Median follow-up was 5.1 years (IQR ⫽ 3.4 to 6.9 years). At baseline, none of the subjects had occlusal caries experience in a third molar; 51% of subjects had at least 1 PD ⱖ4 mm in a third molar region. At follow-up, 27% of the subjects had occlusal caries experience in at least 1 third molar that erupted to the occlusal plane; 61% had at least 1 PD ⱖ4 mm in a third molar region. Twenty-nine percent had occlusal caries in at least 1 third molar at the occlusal plane and at least 1 PD ⱖ4 mm in a third molar region. Thirty-seven percent had no third molar occlusal caries experience and all third molar region PD ⬍4 mm. Conclusions: For third molars that erupted “late,” periodontal pathology was more prevalent than occlusal caries. © 2008 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 66:948-953, 2008 Third molars functioning at the occlusal plane and pathology-free can be retained as components of a healthy dentition. When third molar pathology is detected, cli-
nicians often have difficulty deciding whether to recommend treatment or third molar removal. The anatomic location of third molars makes caries treatment techni-
*Dental Student, School of Dentistry, University of North Carolina, Chapel Hill, NC. †Dental Student, School of Dentistry, University of North Carolina, Chapel Hill, NC. ‡Professor, Department of Operative Dentistry, School of Dentistry, University of North Carolina, Chapel Hill, NC. §Dalton L. McMichael Distinguished Professor, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. 储Clinical Associate Professor, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. ¶Professor, Department of Oral and Maxillofacial Surgery and Assistant Dean, College of Dentistry, University of Kentucky, Lexington, KY. **OraPharma Distinguished Professor, Department of Periodon-
tology, School of Dentistry, University of North Carolina, Chapel Hill, NC. ††Professor, Department of Orthodontics, School of Dentistry, University of North Carolina, Chapel Hill, NC. Supported by funding from the Oral and Maxillofacial Surgery Foundation, American Association of Oral and Maxillofacial Surgeons, and Dental Foundation of North Carolina. Address correspondence and reprint requests to Dr White: Department of Oral and Maxillofacial Surgery, University of North Carolina, CB 7450, Chapel Hill, NC 27599; e-mail: [email protected] © 2008 American Association of Oral and Maxillofacial Surgeons
0278-2391/08/6605-0018$34.00/0 doi:10.1016/j.joms.2007.11.013
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cally more difficult in these teeth compared with other teeth. A similar dilemma exists when asymptomatic periodontal pathology affecting third molars is detected. Adding to the complexity of treatment decisions, patients have less success with home care directed toward third molars. Thus, the biofilm containing bacteria etiologic for caries or periodontal pathology is less likely to be altered or removed. The problem of an appropriate recommendation is more vexing for young adults with unerupted third molars, particularly those in whom jaw growth is complete. Patients with unerupted third molars want advice about retaining these third molars, which may erupt to the occlusal plane over time. Estimating whether third molars may erupt to a functional position and be pathology-free remains difficult, because of the lack of longitudinal data on pathology affecting third molars. These data would allow clinicians to better define the options open to affected patients: third molar removal or third molar retention with clinical monitoring over time. For subjects under age 25, Shugars et al1 reported that occlusal caries experience for third molars at the occlusal plane was 19%. Phillips et al2 reported that subjects at least 25 years old whose third molars erupted at follow-up 6 years after baseline were more likely to have at least one periodontal probing depth (PD) ⱖ4 mm in a third molar region compared with younger subjects with erupting third molars (76% vs 35%). No caries data were reported for the subjects of Phillips et al,2 and no periodontal data were reported for those of Shugars et al.1 Thus, no current data exist for the same subjects on periodontal pathology in the third molar region and occlusal caries experience for third molars erupting late in the occlusal plane after jaw growth is complete. The present analysis was designed to assess the prevalence in young adults of occlusal caries experience for third molars erupting over time after enrollment, as well as the prevalence of periodontal pathology at follow-up in the third molar region for the same subjects.
Patients and Methods The data for these analyses are derived from a larger project involving volunteer subjects enrolled with 4 asymptomatic third molars with adjacent second molars in an institutional review board–approved study at 2 academic clinical centers (University of Kentucky and the University of North Carolina). Subjects were enrolled over a 4-year period ending in 2002, and were asked to retain their third molars for the duration of the study. Inclusion criteria for the larger trial dictated that subjects be healthy (American Society of
949 Anesthesiologists physical status risk classification I, II) as determined by the clinician examiner, and be between the ages of 14 and 45 years at baseline. Subjects who had the most severe form of periodontal disease determined by clinical exam (American Academy of Periodontology IV) reported being pregnant, had a history of psychiatric treatment within the past 12 months, or reported having taken any systemic antibiotics within the previous 3 months were excluded from participation. The subjects did not receive their routine dental care as part of the study, but were encouraged to seek regular care from a general dentist of their choosing. However, all subjects considered for these analyses had a minimal level of dental care. After the clinical data were collected, all subjects received dental prophylaxis at baseline and at each subsequent visit. The subjects selected from the larger trial for our analyses had to have at least 1 third molar below the occlusal plane at baseline that had erupted to the occlusal plane by follow-up. Third molars at the occlusal plane were considered to be in function. The subjects also had to have a follow-up at least 2 years after baseline data were collected. Demographic data and data assessing oral health were obtained at baseline and longest follow-up for each subject. Panoramic radiographs were obtained at baseline and follow-up to assess the degree of eruption of each third molar as at or below the occlusal plane, as suggested by Hugoson and Kugelberg.3 Clinical data on caries experience were collected for each participant through a visual-tactile examination similar to that used in national child and adult caries studies.4 The presence or absence of occlusal caries experience (carious lesions or restorations) for the third molars at the occlusal plane and on any surface of the first and second molars was charted. The presence of a sealant was recorded as a restoration. In addition to the clinical examination, panoramic radiographs obtained at the same visit were examined for molar restorations. (For additional detail on data collection and data management please see Shugars et al.5) Full-mouth periodontal probing, 6 sites per tooth including the third molars, was conducted to assess periodontal status. Each PD detected with a UNC-15 probe was rounded to the lower whole mm. The third molar region was defined as the 6 PDs around the third molars and the 2 sites on the distal of the second molars. A PD ⱖ4 mm in at least 1 probing site in a third molar region was considered indicative of periodontal pathology.6,7 We report periodontal pathology in the third molar region and third molar caries experience by subject
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FIGURE 1. Flow of subjects from enrollment to analyses. Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
and by jaw. Because of the small sample sizes, we limited the analyses to descriptive statistics only.
Results In the larger trial, 152 of 389 (39%) subjects had at least 1 third molar below the occlusal plane at enrollment (Fig 1). Thirty-two percent of these subjects (49 of 152) had at least 1 third molar erupt to the occlusal plane between baseline and longest follow-up. Most of the 49 subjects for these analyses were female (51%) and Caucasian (76%) (Table 1). The subjects were young adults (median age, 20.5 years; interquartile range [IQR] ⫽ 18.4 to 24.1 years) and were well educated (82% with at least a high school education). Median follow-up from baseline was 5.1 years (IQR ⫽ 3.4 to 6.9 years). At baseline, 55% of the subjects had 4 third molars below the occlusal plane. Only 12% had only 1 third
molar below the occlusal plane. Approximately 5 years later, the anatomic position of the third molars had changed markedly. In 51% of the subjects, all 4 third molars were at the occlusal plane; only 25% of subjects had 3 third molars below the occlusal plane. One hundred of the 156 (64%) unerupted third molars at baseline reached the occlusal plane over time, divided almost equally between the maxilla and mandible (Fig 1; Table 2). Only 40 of the 196 (20%) third molars in the 49 study subjects were at the occlusal plane at both baseline and follow-up. None of the subjects had caries detected in any third molar at baseline. More than one quarter of the subjects (13 of 49; 27%), had at least 1 erupting third molar with caries experience at longest follow-up (Table 3). Three of the 13 subjects (23%) had caries experience in more than 1 erupting third molar. Only 2 of the 13 subjects (15%) with caries experience in
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Table 1. DEMOGRAPHIC CHARACTERISTICS AND DURATION OF FOLLOW-UP FOR SUBJECTS WITH AT LEAST 1 THIRD MOLAR BELOW THE OCCLUSAL PLANE AT BASELINE, ERUPTING TO THE OCCLUSAL PLANE AT LONGEST FOLLOW-UP (N ⴝ 49)
Subjects n
(%)
Female Male
25 24
(51) (49)
Caucasian African-American Other
37 8 4
(76) (16) (8)
Education At least high school At least college graduate
40 18
(82) (37)
Tobacco use Yes No
6 35
(15) (85)
Age at Enrollment, years Follow-up, years
Median (IQR) 20.5 (18.4 to 24.1) 5.1 (3.4 to 6.9)
NOTE. Data are incomplete for 8 subjects. Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
erupting third molars also had at least 1 first or second molar with caries experience (data not shown). A PD ⱖ4 mm in the third molar region in the same quadrant was more prevalent at follow-up if a third molar had erupted to the occlusal plane after baseline than for third molars below the occlusal plane at follow-up (54% vs 18%). Periodontal pathology occurred more frequently in the mandibular third molar region than in the maxillary third molar region (61% vs 15%) (periodontal data by quadrant not displayed). Periodontal pathology in the third molar region was more prevalent than occlusal caries experience. Fifty-one percent of subjects had at least 1 PD ⱖ4 mm at baseline. Sixty-one percent of subjects had at least 1 PD ⱖ4 mm in a third molar region at follow-up (Table 4). At longest follow-up, 37% of the subjects had no occlusal caries experience or any PD ⱖ4 mm in a third molar region (Table 4). Twenty-nine percent of
subjects had both third molar occlusal caries and at least 1 PD ⱖ4 mm in a third molar region.
Discussion The most important clinically relevant finding from our analyses of young adult subjects whose third molars erupted late to the occlusal plane was that periodontal pathology (at least 1 PD ⱖ4 mm) was twice as likely to be detected in a third molar region (61% of subjects) than third molar occlusal caries experience (31% of subjects). At follow-up, the prevalence of periodontal pathology with erupting third molars was almost 3 times greater compared with third molars below the occlusal plane. In the only population study addressing age and third molar eruption, Rantanen8 reported that frequency of eruption was highest at age 19.5 years. By age 23, only 2% to 3% of third molars continued to erupt. We considered that third molars had erupted to the occlusal plane “late” after the peak eruption period in our subjects with an average age over 20 years and likely after jaw growth was complete. Reports on caries affecting third molars are limited. Shugars et al1,5 investigated the prevalence of third molar occlusal caries experience for subjects under 25 years old with at least 1 third molar at the occlusal plane. The age range of subjects at baseline was similar in our study and in the study of Shugars et al; however, most subjects in the latter study (74%) had 4 third molars at the occlusal plane, and only 8% had only 1 third molar at the occlusal plane.5 At baseline, more than half of the subjects that we studied (55%) had all 4 third molars below the occlusal plane. But third molar position relative to the occlusal plane changed after baseline; 51% of our subjects had four third molars at the occlusal plane at follow-up. A larger percentage of subjects in our study had occlusal caries experience on a third molar that erupted to the occlusal plane “late” during the median 5-year follow-up period compared with those studied by Shugars et al (27% vs. 19%).5 It is plausible that an anatomic position lower than the occlusal plane for these late-erupting third molars made these erupting teeth more susceptible to caries pathogens in the
Table 2. FREQUENCIES OF THIRD MOLAR POSITION RELATIVE TO THE OCCLUSAL PLANE AT FOLLOW-UP
Maxilla (n ⫽ 98) Mandible (n ⫽ 98) Total (n ⫽ 196)
At the Occlusal Plane: Baseline and Follow-Up, n (%)
Erupting to the Occlusal Plane: Baseline to Follow-up, n (%)
Below the Occlusal Plane at Follow-up, n (%)
18 (18%) 22 (22%) 40 (20%)
54 (55%) 46 (47%) 100 (51%)
26 (27%) 30 (31%) 56 (29%)
Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
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PATHOLOGY AND ERUPTING THIRD MOLARS
Table 3. SUBJECTS’ THIRD MOLAR CARIES EXPERIENCE AT LONGEST FOLLOW-UP, N ⴝ 49
No third molar with caries experience At least 1 third molar with caries experience At least 2 third molars with caries experience
Caries Experience for all Third Molars at Follow-Up, n (%)
Caries Experience for Third Molars Erupting Between Baseline and Follow-Up n (%)
34 (69%)
36 (73%)
15 (31%)
13 (27%)
4 (8%)
3 (6%)
Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
biofilm colonized on the occlusal surface. The comparison between caries prevalence in “early” versus “late” erupting third molars merits further study. Few of our study subjects (8%) had occlusal caries experience on more than 1 third molar. Shugars et al1 also reported that subjects’ caries experience in those under 25 years old involving more than 1 third molar was low. Both mandibular third molars in Shugars’ subjects were affected in only 6% of subjects, and both maxillary third molars were affected in only 1%. In our subjects, occlusal caries experience in third molars at follow-up was generally limited to these teeth. Only 2 subjects (4%) had caries experience on a third molar and a first or second molar. These data contrast with data reported by Shugars et al.5 In all but 5% of their affected subjects, caries experience was detected on third molars and at least 1 first or second molar. We cannot account for these differences. The prevalence of periodontal pathology in our study subjects was similar to that reported by Blakey et al9 in a related study from the larger clinical trial. For 195 subjects with a median 6 years of follow-up, 64% had at least 1 PD ⱖ4 mm in a third molar region. For our subset of 49 subjects; 61% had at least 1 PD ⱖ4 mm in a third molar region at median 5 year follow-up, almost double the overall third molar caries experience of 31%. These data suggest that third molar periodontal pathology may be more prevalent than caries experience in young adults, findings that may surprise clinicians. Partially erupted third molars that are not clinically accessible may change anatomic position such that PDs can be measured before the teeth erupt to the occlusal plane. Increased periodontal PDs around these teeth are termed “pseudopockets” by some cli-
nicians. A problem arises only if clinicians consider “pseudopockets” to be a benign condition that is inconsequential to oral health. Once third molars can be probed, the teeth are exposed to the oral cavity with the subsequent colonization of oral flora in a nonsheddable biofilm on the tooth surface. Following the current biological model, periodontal health or periodontal pathology results from the interaction between pathogenic bacteria colonized in the biofilm on the nonsheddable tooth surface and the immune response to the bacteria and their products at the adjacent soft tissue, the biofilm– gingival interface (BGI).10 “Orange” cluster pathogens are facultative anaerobes; “red” cluster pathogens are strict anaerobes.11 Deepening PD at the BGI is associated with anaerobic conditions. Elevated counts of “orange” cluster periodontal pathogens are most often associated with PD 3 to 4 mm and elevated counts of both “red” and “orange” cluster pathogens are most often associated with PD at least 4 mm. Elevated counts of “orange” and “red” cluster pathogens are considered risk factors for periodontal pathology. Data from our collective clinical studies in young adults are compatible with and add credence to the current biological model of periodontal pathology. Our data support the emerging concept that periodontal PDs are more reliable risk markers or risk indicators for periodontal pathology in young adults than periodontal attachment loss or alveolar bone loss, traditional clinical indicators for disease in older adults.7,12-16 Clearly, the concept that “pseudopockets” detected with third molars are benign is outmoded, considering the current biological model of periodontal pathology as it applies to third molars. Continuing to assume that all “pseudopockets” are not detrimental may pose a risk to oral health in affected individuals. Not everyone who reaches adulthood will be affected by third molar caries experience or periodon-
Table 4. FREQUENCY OF SUBJECTS ACCORDING TO CARIES EXPERIENCE FOR AT LEAST 1 THIRD MOLAR AT THE OCCLUSAL PLANE AT FOLLOW-UP AND PERIODONTAL PATHOLOGY, AT LEAST ONE PERIODONTAL PROBING DEPTH >4 MM IN AT LEAST ONE THIRD MOLAR REGION
Caries Experience in At Least 1 Periodontal at Least 1 Third PD ⱖ4 mm in any Molar Erupting Third Molar Region Between Baseline and Follow-up Total, n (%) No, n (%) Yes, n (%) No Yes Total
18 (37%) 1 (2%) 19 (39%)
16 (33%) 14 (29%) 30 (61%)
34 (69%) 15 (31%) 49 (100%)
Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
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tal pathology. More than 1/3 of the young adults that we studied had no detected occlusal caries or PD ⱖ4 mm in a third molar region. Moss et al17 also found that 21% of seniors with a mean age of 73 years and at least 1 retained third molar had no evidence of third molar occlusal caries or periodontal pathology. In Moss et al’s analyses, third molar caries experience affected 28% of the 342 subjects studied with visible third molars, similar to our overall prevalence of third molar occlusal caries (31% of subjects).17 Congruent with our findings, periodontal pathology was more prevalent than third molar caries in the senior subjects’ experience of Moss et al.17 Using clinical attachment loss of at least 3 mm as a risk marker, 68% of Moss et al’s senior subjects were affected with periodontal pathology, compared with 61% of our subjects with at least 1 PD ⱖ4 mm. These data from subjects in younger and older age ranges should be useful to clinicians advising patients about the options for third molar treatment. Our findings have some limitations. Our study subjects and those in the larger longitudinal trial are a diverse group of young adults retaining asymptomatic third molars over time, but they are not a sample representative of the US population as a whole. Asian and Hispanic subjects may be under-represented, and education levels are higher. As discussed by Shugars et al,5 our detection methods for caries could either underestimate or overestimate third molar caries experience for a larger population. However, the same methods of detection of caries experience that we used were also used for the larger sample analyzed by Shugars et al1,5 and also for the senior adults analyzed by Moss et al.17 Few population studies have assessed periodontal pathology on third molars. Thus the data that we report on the prevalence of periodontal pathology in a third molar region also may be greater or less in the US population. Keeping these limitations in mind, we suggest that our data can assist clinicians and their patients in making decisions concerning treatment of late-erupting third molars in young adults. Acknowledgments The authors thank Debora Price for assisting with the data management for this project, and Sharon Williams, Robin Hambly,
Donna Mischel, Charlotte Stokley, and Tiffany Hambright for serving as clinical coordinators.
References 1. Shugars DA, Elter JR, Jacks TM, et al: Incidence of occlusal dental caries in asymptomatic third molars. J Oral Maxillofac Surg 63:341, 2005 2. Phillips C, Norman J, Jaskolka M, et al: Changes over time in position and periodontal probing status of retained third molars. In press J Oral Maxillofac Surg 65:2011, 2007 3. Hugoson A, Kugelberg CF: The prevalence of third molars in a Swedish population: An epidemiologic study. Community Dent Health 5:121, 1988 4. Bader JD, Shugars DA, Rozier RG: Relationship between epidemiologic coronal caries assessment and practitioner’s treatment recommendations in adults. Community Dent Oral Epidemiol 21:96, 1993 5. Shugars DA, Jacks TM, White RP Jr, et al: Occlusal caries in patients with asymptomatic third molars. J Oral Maxillofac Surg 62:973, 2004 6. 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 7. White RP Jr, Offenbacher S, Blakey GH, et al: Chronic oral inflammation and the progression of periodontal pathology in the third molar region. J Oral Maxillofac Surg 64:880, 2006 8. Rantanen AV: The age of eruption of the third molar teeth. Acta Odontol Scand 25 (Suppl):48, 1967 9. 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 10. Offenbacher S, Barros S, Singer B, et al: Periodontal disease at the biofilm-gingival interface (BGI). J Periodontol 78:1911, 2007 11. Socransky SS, Haffajee AD: Periodontal microbial ecology. Periodontol 2000 38:135, 2005 12. White RP Jr, Madianos PN, Offenbacher S, et al: Microbial complexes detected in the second/third molar region in patients with asymptomatic third molars. J Oral Maxillofac Surg 60:1234, 2002 13. White RP Jr, Offenbacher S, Blakey GH, et al: Chronic oral inflammation and the progression of periodontal pathology in the third molar region. J Oral Maxillofac Surg 64:880, 2006 14. Moss KL, Mauriello SM, Ruvo AT, et al: Reliability of third molar probing measures and the systemic impact of periodontal pathology. J Oral Maxillofac Surg 64:652, 2006 15. Moss KL, Ruvo AT, Offenbacher S, et al: Third molars and progression of periodontal pathology during pregnancy. J Oral Maxillofac Surg 65:1065, 2007 16. 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 17. Moss KL, Beck JD, Mauriello SM, et al: Third molar periodontal pathology and caries in senior adults. J Oral Maxillofac Surg 65:103, 2007
Caries Experience and Periodontal Pathology in Erupting Third Molars Nazir Ahmad,* Savannah Gelesko,† Daniel Shugars, DDS, PhD, MPH,‡ Raymond P. White, Jr, DDS, PhD,§ George Blakey, DDS,储 Richard H. Haug, DDS,¶ Steven Offenbacher, DDS, PhD,** and Ceib Phillips, PhD, MPH†† Purpose: This study was conducted to document the prevalence of occlusal caries experience and
periodontal pathology for erupting third molars in young adults. Patients and Methods: The data are from 49 subjects enrolled in an institutional review board–approved trial with at least one third molar below the occlusal plane at baseline that erupted by longest follow-up. Teeth were considered erupted if they reached the occlusal plane. Caries experience on the occlusal surface of third molars was assessed by a visual-tactile examination. At least 1 periodontal probing depth (PD) ⱖ4 mm in the third molar region was considered indicative of periodontal pathology. The third molar region was defined as the 6 probing sites around third molars and 2 sites on the distal of second molars. The prevalence of third molar caries experience and periodontal pathology at longest follow-up was assessed. Results: Most of the 49 subjects were female (51%), Caucasian (76%), and educated at least through high school (82%). Median age was 20.5 years (interquartile range [IQR] 18.4 to 24.1 years). Median follow-up was 5.1 years (IQR ⫽ 3.4 to 6.9 years). At baseline, none of the subjects had occlusal caries experience in a third molar; 51% of subjects had at least 1 PD ⱖ4 mm in a third molar region. At follow-up, 27% of the subjects had occlusal caries experience in at least 1 third molar that erupted to the occlusal plane; 61% had at least 1 PD ⱖ4 mm in a third molar region. Twenty-nine percent had occlusal caries in at least 1 third molar at the occlusal plane and at least 1 PD ⱖ4 mm in a third molar region. Thirty-seven percent had no third molar occlusal caries experience and all third molar region PD ⬍4 mm. Conclusions: For third molars that erupted “late,” periodontal pathology was more prevalent than occlusal caries. © 2008 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 66:948-953, 2008 Third molars functioning at the occlusal plane and pathology-free can be retained as components of a healthy dentition. When third molar pathology is detected, cli-
nicians often have difficulty deciding whether to recommend treatment or third molar removal. The anatomic location of third molars makes caries treatment techni-
*Dental Student, School of Dentistry, University of North Carolina, Chapel Hill, NC. †Dental Student, School of Dentistry, University of North Carolina, Chapel Hill, NC. ‡Professor, Department of Operative Dentistry, School of Dentistry, University of North Carolina, Chapel Hill, NC. §Dalton L. McMichael Distinguished Professor, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. 储Clinical Associate Professor, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. ¶Professor, Department of Oral and Maxillofacial Surgery and Assistant Dean, College of Dentistry, University of Kentucky, Lexington, KY. **OraPharma Distinguished Professor, Department of Periodon-
tology, School of Dentistry, University of North Carolina, Chapel Hill, NC. ††Professor, Department of Orthodontics, School of Dentistry, University of North Carolina, Chapel Hill, NC. Supported by funding from the Oral and Maxillofacial Surgery Foundation, American Association of Oral and Maxillofacial Surgeons, and Dental Foundation of North Carolina. Address correspondence and reprint requests to Dr White: Department of Oral and Maxillofacial Surgery, University of North Carolina, CB 7450, Chapel Hill, NC 27599; e-mail: [email protected] © 2008 American Association of Oral and Maxillofacial Surgeons
0278-2391/08/6605-0018$34.00/0 doi:10.1016/j.joms.2007.11.013
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cally more difficult in these teeth compared with other teeth. A similar dilemma exists when asymptomatic periodontal pathology affecting third molars is detected. Adding to the complexity of treatment decisions, patients have less success with home care directed toward third molars. Thus, the biofilm containing bacteria etiologic for caries or periodontal pathology is less likely to be altered or removed. The problem of an appropriate recommendation is more vexing for young adults with unerupted third molars, particularly those in whom jaw growth is complete. Patients with unerupted third molars want advice about retaining these third molars, which may erupt to the occlusal plane over time. Estimating whether third molars may erupt to a functional position and be pathology-free remains difficult, because of the lack of longitudinal data on pathology affecting third molars. These data would allow clinicians to better define the options open to affected patients: third molar removal or third molar retention with clinical monitoring over time. For subjects under age 25, Shugars et al1 reported that occlusal caries experience for third molars at the occlusal plane was 19%. Phillips et al2 reported that subjects at least 25 years old whose third molars erupted at follow-up 6 years after baseline were more likely to have at least one periodontal probing depth (PD) ⱖ4 mm in a third molar region compared with younger subjects with erupting third molars (76% vs 35%). No caries data were reported for the subjects of Phillips et al,2 and no periodontal data were reported for those of Shugars et al.1 Thus, no current data exist for the same subjects on periodontal pathology in the third molar region and occlusal caries experience for third molars erupting late in the occlusal plane after jaw growth is complete. The present analysis was designed to assess the prevalence in young adults of occlusal caries experience for third molars erupting over time after enrollment, as well as the prevalence of periodontal pathology at follow-up in the third molar region for the same subjects.
Patients and Methods The data for these analyses are derived from a larger project involving volunteer subjects enrolled with 4 asymptomatic third molars with adjacent second molars in an institutional review board–approved study at 2 academic clinical centers (University of Kentucky and the University of North Carolina). Subjects were enrolled over a 4-year period ending in 2002, and were asked to retain their third molars for the duration of the study. Inclusion criteria for the larger trial dictated that subjects be healthy (American Society of
949 Anesthesiologists physical status risk classification I, II) as determined by the clinician examiner, and be between the ages of 14 and 45 years at baseline. Subjects who had the most severe form of periodontal disease determined by clinical exam (American Academy of Periodontology IV) reported being pregnant, had a history of psychiatric treatment within the past 12 months, or reported having taken any systemic antibiotics within the previous 3 months were excluded from participation. The subjects did not receive their routine dental care as part of the study, but were encouraged to seek regular care from a general dentist of their choosing. However, all subjects considered for these analyses had a minimal level of dental care. After the clinical data were collected, all subjects received dental prophylaxis at baseline and at each subsequent visit. The subjects selected from the larger trial for our analyses had to have at least 1 third molar below the occlusal plane at baseline that had erupted to the occlusal plane by follow-up. Third molars at the occlusal plane were considered to be in function. The subjects also had to have a follow-up at least 2 years after baseline data were collected. Demographic data and data assessing oral health were obtained at baseline and longest follow-up for each subject. Panoramic radiographs were obtained at baseline and follow-up to assess the degree of eruption of each third molar as at or below the occlusal plane, as suggested by Hugoson and Kugelberg.3 Clinical data on caries experience were collected for each participant through a visual-tactile examination similar to that used in national child and adult caries studies.4 The presence or absence of occlusal caries experience (carious lesions or restorations) for the third molars at the occlusal plane and on any surface of the first and second molars was charted. The presence of a sealant was recorded as a restoration. In addition to the clinical examination, panoramic radiographs obtained at the same visit were examined for molar restorations. (For additional detail on data collection and data management please see Shugars et al.5) Full-mouth periodontal probing, 6 sites per tooth including the third molars, was conducted to assess periodontal status. Each PD detected with a UNC-15 probe was rounded to the lower whole mm. The third molar region was defined as the 6 PDs around the third molars and the 2 sites on the distal of the second molars. A PD ⱖ4 mm in at least 1 probing site in a third molar region was considered indicative of periodontal pathology.6,7 We report periodontal pathology in the third molar region and third molar caries experience by subject
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FIGURE 1. Flow of subjects from enrollment to analyses. Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
and by jaw. Because of the small sample sizes, we limited the analyses to descriptive statistics only.
Results In the larger trial, 152 of 389 (39%) subjects had at least 1 third molar below the occlusal plane at enrollment (Fig 1). Thirty-two percent of these subjects (49 of 152) had at least 1 third molar erupt to the occlusal plane between baseline and longest follow-up. Most of the 49 subjects for these analyses were female (51%) and Caucasian (76%) (Table 1). The subjects were young adults (median age, 20.5 years; interquartile range [IQR] ⫽ 18.4 to 24.1 years) and were well educated (82% with at least a high school education). Median follow-up from baseline was 5.1 years (IQR ⫽ 3.4 to 6.9 years). At baseline, 55% of the subjects had 4 third molars below the occlusal plane. Only 12% had only 1 third
molar below the occlusal plane. Approximately 5 years later, the anatomic position of the third molars had changed markedly. In 51% of the subjects, all 4 third molars were at the occlusal plane; only 25% of subjects had 3 third molars below the occlusal plane. One hundred of the 156 (64%) unerupted third molars at baseline reached the occlusal plane over time, divided almost equally between the maxilla and mandible (Fig 1; Table 2). Only 40 of the 196 (20%) third molars in the 49 study subjects were at the occlusal plane at both baseline and follow-up. None of the subjects had caries detected in any third molar at baseline. More than one quarter of the subjects (13 of 49; 27%), had at least 1 erupting third molar with caries experience at longest follow-up (Table 3). Three of the 13 subjects (23%) had caries experience in more than 1 erupting third molar. Only 2 of the 13 subjects (15%) with caries experience in
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Table 1. DEMOGRAPHIC CHARACTERISTICS AND DURATION OF FOLLOW-UP FOR SUBJECTS WITH AT LEAST 1 THIRD MOLAR BELOW THE OCCLUSAL PLANE AT BASELINE, ERUPTING TO THE OCCLUSAL PLANE AT LONGEST FOLLOW-UP (N ⴝ 49)
Subjects n
(%)
Female Male
25 24
(51) (49)
Caucasian African-American Other
37 8 4
(76) (16) (8)
Education At least high school At least college graduate
40 18
(82) (37)
Tobacco use Yes No
6 35
(15) (85)
Age at Enrollment, years Follow-up, years
Median (IQR) 20.5 (18.4 to 24.1) 5.1 (3.4 to 6.9)
NOTE. Data are incomplete for 8 subjects. Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
erupting third molars also had at least 1 first or second molar with caries experience (data not shown). A PD ⱖ4 mm in the third molar region in the same quadrant was more prevalent at follow-up if a third molar had erupted to the occlusal plane after baseline than for third molars below the occlusal plane at follow-up (54% vs 18%). Periodontal pathology occurred more frequently in the mandibular third molar region than in the maxillary third molar region (61% vs 15%) (periodontal data by quadrant not displayed). Periodontal pathology in the third molar region was more prevalent than occlusal caries experience. Fifty-one percent of subjects had at least 1 PD ⱖ4 mm at baseline. Sixty-one percent of subjects had at least 1 PD ⱖ4 mm in a third molar region at follow-up (Table 4). At longest follow-up, 37% of the subjects had no occlusal caries experience or any PD ⱖ4 mm in a third molar region (Table 4). Twenty-nine percent of
subjects had both third molar occlusal caries and at least 1 PD ⱖ4 mm in a third molar region.
Discussion The most important clinically relevant finding from our analyses of young adult subjects whose third molars erupted late to the occlusal plane was that periodontal pathology (at least 1 PD ⱖ4 mm) was twice as likely to be detected in a third molar region (61% of subjects) than third molar occlusal caries experience (31% of subjects). At follow-up, the prevalence of periodontal pathology with erupting third molars was almost 3 times greater compared with third molars below the occlusal plane. In the only population study addressing age and third molar eruption, Rantanen8 reported that frequency of eruption was highest at age 19.5 years. By age 23, only 2% to 3% of third molars continued to erupt. We considered that third molars had erupted to the occlusal plane “late” after the peak eruption period in our subjects with an average age over 20 years and likely after jaw growth was complete. Reports on caries affecting third molars are limited. Shugars et al1,5 investigated the prevalence of third molar occlusal caries experience for subjects under 25 years old with at least 1 third molar at the occlusal plane. The age range of subjects at baseline was similar in our study and in the study of Shugars et al; however, most subjects in the latter study (74%) had 4 third molars at the occlusal plane, and only 8% had only 1 third molar at the occlusal plane.5 At baseline, more than half of the subjects that we studied (55%) had all 4 third molars below the occlusal plane. But third molar position relative to the occlusal plane changed after baseline; 51% of our subjects had four third molars at the occlusal plane at follow-up. A larger percentage of subjects in our study had occlusal caries experience on a third molar that erupted to the occlusal plane “late” during the median 5-year follow-up period compared with those studied by Shugars et al (27% vs. 19%).5 It is plausible that an anatomic position lower than the occlusal plane for these late-erupting third molars made these erupting teeth more susceptible to caries pathogens in the
Table 2. FREQUENCIES OF THIRD MOLAR POSITION RELATIVE TO THE OCCLUSAL PLANE AT FOLLOW-UP
Maxilla (n ⫽ 98) Mandible (n ⫽ 98) Total (n ⫽ 196)
At the Occlusal Plane: Baseline and Follow-Up, n (%)
Erupting to the Occlusal Plane: Baseline to Follow-up, n (%)
Below the Occlusal Plane at Follow-up, n (%)
18 (18%) 22 (22%) 40 (20%)
54 (55%) 46 (47%) 100 (51%)
26 (27%) 30 (31%) 56 (29%)
Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
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Table 3. SUBJECTS’ THIRD MOLAR CARIES EXPERIENCE AT LONGEST FOLLOW-UP, N ⴝ 49
No third molar with caries experience At least 1 third molar with caries experience At least 2 third molars with caries experience
Caries Experience for all Third Molars at Follow-Up, n (%)
Caries Experience for Third Molars Erupting Between Baseline and Follow-Up n (%)
34 (69%)
36 (73%)
15 (31%)
13 (27%)
4 (8%)
3 (6%)
Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
biofilm colonized on the occlusal surface. The comparison between caries prevalence in “early” versus “late” erupting third molars merits further study. Few of our study subjects (8%) had occlusal caries experience on more than 1 third molar. Shugars et al1 also reported that subjects’ caries experience in those under 25 years old involving more than 1 third molar was low. Both mandibular third molars in Shugars’ subjects were affected in only 6% of subjects, and both maxillary third molars were affected in only 1%. In our subjects, occlusal caries experience in third molars at follow-up was generally limited to these teeth. Only 2 subjects (4%) had caries experience on a third molar and a first or second molar. These data contrast with data reported by Shugars et al.5 In all but 5% of their affected subjects, caries experience was detected on third molars and at least 1 first or second molar. We cannot account for these differences. The prevalence of periodontal pathology in our study subjects was similar to that reported by Blakey et al9 in a related study from the larger clinical trial. For 195 subjects with a median 6 years of follow-up, 64% had at least 1 PD ⱖ4 mm in a third molar region. For our subset of 49 subjects; 61% had at least 1 PD ⱖ4 mm in a third molar region at median 5 year follow-up, almost double the overall third molar caries experience of 31%. These data suggest that third molar periodontal pathology may be more prevalent than caries experience in young adults, findings that may surprise clinicians. Partially erupted third molars that are not clinically accessible may change anatomic position such that PDs can be measured before the teeth erupt to the occlusal plane. Increased periodontal PDs around these teeth are termed “pseudopockets” by some cli-
nicians. A problem arises only if clinicians consider “pseudopockets” to be a benign condition that is inconsequential to oral health. Once third molars can be probed, the teeth are exposed to the oral cavity with the subsequent colonization of oral flora in a nonsheddable biofilm on the tooth surface. Following the current biological model, periodontal health or periodontal pathology results from the interaction between pathogenic bacteria colonized in the biofilm on the nonsheddable tooth surface and the immune response to the bacteria and their products at the adjacent soft tissue, the biofilm– gingival interface (BGI).10 “Orange” cluster pathogens are facultative anaerobes; “red” cluster pathogens are strict anaerobes.11 Deepening PD at the BGI is associated with anaerobic conditions. Elevated counts of “orange” cluster periodontal pathogens are most often associated with PD 3 to 4 mm and elevated counts of both “red” and “orange” cluster pathogens are most often associated with PD at least 4 mm. Elevated counts of “orange” and “red” cluster pathogens are considered risk factors for periodontal pathology. Data from our collective clinical studies in young adults are compatible with and add credence to the current biological model of periodontal pathology. Our data support the emerging concept that periodontal PDs are more reliable risk markers or risk indicators for periodontal pathology in young adults than periodontal attachment loss or alveolar bone loss, traditional clinical indicators for disease in older adults.7,12-16 Clearly, the concept that “pseudopockets” detected with third molars are benign is outmoded, considering the current biological model of periodontal pathology as it applies to third molars. Continuing to assume that all “pseudopockets” are not detrimental may pose a risk to oral health in affected individuals. Not everyone who reaches adulthood will be affected by third molar caries experience or periodon-
Table 4. FREQUENCY OF SUBJECTS ACCORDING TO CARIES EXPERIENCE FOR AT LEAST 1 THIRD MOLAR AT THE OCCLUSAL PLANE AT FOLLOW-UP AND PERIODONTAL PATHOLOGY, AT LEAST ONE PERIODONTAL PROBING DEPTH >4 MM IN AT LEAST ONE THIRD MOLAR REGION
Caries Experience in At Least 1 Periodontal at Least 1 Third PD ⱖ4 mm in any Molar Erupting Third Molar Region Between Baseline and Follow-up Total, n (%) No, n (%) Yes, n (%) No Yes Total
18 (37%) 1 (2%) 19 (39%)
16 (33%) 14 (29%) 30 (61%)
34 (69%) 15 (31%) 49 (100%)
Ahmad et al. Pathology and Erupting Third Molars. J Oral Maxillofac Surg 2008.
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tal pathology. More than 1/3 of the young adults that we studied had no detected occlusal caries or PD ⱖ4 mm in a third molar region. Moss et al17 also found that 21% of seniors with a mean age of 73 years and at least 1 retained third molar had no evidence of third molar occlusal caries or periodontal pathology. In Moss et al’s analyses, third molar caries experience affected 28% of the 342 subjects studied with visible third molars, similar to our overall prevalence of third molar occlusal caries (31% of subjects).17 Congruent with our findings, periodontal pathology was more prevalent than third molar caries in the senior subjects’ experience of Moss et al.17 Using clinical attachment loss of at least 3 mm as a risk marker, 68% of Moss et al’s senior subjects were affected with periodontal pathology, compared with 61% of our subjects with at least 1 PD ⱖ4 mm. These data from subjects in younger and older age ranges should be useful to clinicians advising patients about the options for third molar treatment. Our findings have some limitations. Our study subjects and those in the larger longitudinal trial are a diverse group of young adults retaining asymptomatic third molars over time, but they are not a sample representative of the US population as a whole. Asian and Hispanic subjects may be under-represented, and education levels are higher. As discussed by Shugars et al,5 our detection methods for caries could either underestimate or overestimate third molar caries experience for a larger population. However, the same methods of detection of caries experience that we used were also used for the larger sample analyzed by Shugars et al1,5 and also for the senior adults analyzed by Moss et al.17 Few population studies have assessed periodontal pathology on third molars. Thus the data that we report on the prevalence of periodontal pathology in a third molar region also may be greater or less in the US population. Keeping these limitations in mind, we suggest that our data can assist clinicians and their patients in making decisions concerning treatment of late-erupting third molars in young adults. Acknowledgments The authors thank Debora Price for assisting with the data management for this project, and Sharon Williams, Robin Hambly,
Donna Mischel, Charlotte Stokley, and Tiffany Hambright for serving as clinical coordinators.
References 1. Shugars DA, Elter JR, Jacks TM, et al: Incidence of occlusal dental caries in asymptomatic third molars. J Oral Maxillofac Surg 63:341, 2005 2. Phillips C, Norman J, Jaskolka M, et al: Changes over time in position and periodontal probing status of retained third molars. In press J Oral Maxillofac Surg 65:2011, 2007 3. Hugoson A, Kugelberg CF: The prevalence of third molars in a Swedish population: An epidemiologic study. Community Dent Health 5:121, 1988 4. Bader JD, Shugars DA, Rozier RG: Relationship between epidemiologic coronal caries assessment and practitioner’s treatment recommendations in adults. Community Dent Oral Epidemiol 21:96, 1993 5. Shugars DA, Jacks TM, White RP Jr, et al: Occlusal caries in patients with asymptomatic third molars. J Oral Maxillofac Surg 62:973, 2004 6. 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 7. White RP Jr, Offenbacher S, Blakey GH, et al: Chronic oral inflammation and the progression of periodontal pathology in the third molar region. J Oral Maxillofac Surg 64:880, 2006 8. Rantanen AV: The age of eruption of the third molar teeth. Acta Odontol Scand 25 (Suppl):48, 1967 9. 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 10. Offenbacher S, Barros S, Singer B, et al: Periodontal disease at the biofilm-gingival interface (BGI). J Periodontol 78:1911, 2007 11. Socransky SS, Haffajee AD: Periodontal microbial ecology. Periodontol 2000 38:135, 2005 12. White RP Jr, Madianos PN, Offenbacher S, et al: Microbial complexes detected in the second/third molar region in patients with asymptomatic third molars. J Oral Maxillofac Surg 60:1234, 2002 13. White RP Jr, Offenbacher S, Blakey GH, et al: Chronic oral inflammation and the progression of periodontal pathology in the third molar region. J Oral Maxillofac Surg 64:880, 2006 14. Moss KL, Mauriello SM, Ruvo AT, et al: Reliability of third molar probing measures and the systemic impact of periodontal pathology. J Oral Maxillofac Surg 64:652, 2006 15. Moss KL, Ruvo AT, Offenbacher S, et al: Third molars and progression of periodontal pathology during pregnancy. J Oral Maxillofac Surg 65:1065, 2007 16. 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 17. Moss KL, Beck JD, Mauriello SM, et al: Third molar periodontal pathology and caries in senior adults. J Oral Maxillofac Surg 65:103, 2007