- Email: [email protected]
Third Molar Region in Subjects With Asymptomatic Third Molars
J Oral Maxillofac Surg 64:189-193, 2006
Progression of Periodontal Disease in the Second/Third Molar Region in Subjects With Asymptomatic Third Molars George H. Blakey, DDS,* M. Thomas Jacks, DDS,† Steven Offenbacher, DDS, PhD,‡ Paige E. Nance, DDS,§ Ceib Phillips, PhD,储 Richard H. Haug, DDS,¶ and Raymond P. White, Jr, DDS, PhD# Purpose: To assess the change in periodontal status over time by periodontal probing depth (PD) in the
third molar region. Subjects and Methods: The data for these analyses are part of a study of subjects enrolled with 4
asymptomatic third molars with adjacent second molars in an institutional review board-approved longitudinal trial. Full mouth periodontal probing was conducted to determine periodontal status at baseline and follow-up. Panoramic radiographs were analyzed for angulation and degree of eruption of third molars. Subjects were categorized as those who exhibited at least a 2 mm change in periodontal PD between baseline and follow-up in the third molar region, the distal of a second molar or around a third molar, and those who did not exhibit a 2 mm or greater change. Subjects with and without changes in PD were compared with Cochran-Mantel-Haenzsel statistics. Level of significance was set at 0.05. Results: Data from 254 subjects with at least 2 annual follow-up visits were available for analysis. Mean age at baseline was 27.5 years. Median follow-up from baseline to the second follow-up visit was 2.2 years (interquartile range 2.0, 2.6). At enrollment, 59% of the subjects had at least 1 PD ⱖ4 mm in the third molar region, one quarter had a PD ⱖ5 mm. Twenty-four percent of the subjects had at least 1 tooth that had an increased PD ⱖ2 mm in the third molar region at follow-up. If subjects had at least 1 PD ⱖ4 mm at baseline, 38% had at least 1 PD deepen by 2 mm or more at follow-up. Only 3% of those who had all teeth with a PD of less than 4 mm at baseline exhibited a change of ⱖ2 mm (P ⬍ .001). Conclusion: Increased periodontal PDs ⱖ2 mm were often found in the third molar region for asymptomatic subjects with at least 1 PD ⱖ4 mm at enrollment, clinical measures that indicated increased periodontal pathology, and a deteriorating periodontal condition. © 2006 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 64:189-193, 2006 Blakey et al1 reported a higher prevalence of increased periodontal probing depths (PD) in the third molar region than clinicians expected. At baseline, 25% of the sample of 329 subjects enrolled in a longitudinal trial had at least 1 PD ⱖ5 mm in the third
molar region; one third of subjects at least 25 years of age had at least 1 PD ⱖ5 mm. Only 4 subjects had PD ⱖ5 mm anterior to the third molar region. White et al2,3 documented that the same subjects who had a PD ⱖ5 mm at baseline had elevated levels
*Clinical Assistant Professor, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. †Former Senior Resident, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. ‡Ora Pharma Professor, Department of Periodontics, School of Dentistry, University of North Carolina, Chapel Hill, NC. §Clinical Research Fellow, Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. 储Professor, Department of Orthodontics, School of Dentistry, University of North Carolina, Chapel Hill, NC. ¶Professor, Department of Oral and Maxillofacial Surgery, Assistant Dean, College of Dentistry, University of Kentucky, Lexington, KY.
#Dalton L. McMichael Professor, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. Supported in part by the Oral and Maxillofacial Surgery Foundation, American Association of Oral and Maxillofacial Surgeons, and the Dental Foundation of North Carolina. Address correspondence and reprint requests to Dr White: Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC 27599-7450; e-mail: [email protected] © 2006 American Association of Oral and Maxillofacial Surgeons
0278-2391/06/6402-0007$32.00/0 doi:10.1016/j.joms.2005.10.014
189
190 of “orange” and “red” complex periodontal pathogens detected in biofilm samples from the distal of second molars and elevated levels of the gingival crevicular fluid inflammatory mediator, IL-1. These data suggest that retained third molars with periodontal pathology are a source of chronic oral inflammation. Current clinical research continues to focus on the impact of chronic inflammation at remote anatomic sites with cardiovascular disease.4 Chronic oral inflammation associated with periodontal disease has been implicated in increasing the risk for cardiovascular disease as well as for renal insufficiency and preterm birth.5-8 The common denominator for all of these clinical conditions is endothelial cell activation associated with chronic inflammation at remote sites including the oral cavity. Increased PD over time is a clinical measure of an increase in severity of periodontal disease and an increased level of chronic oral inflammation. If periodontal pathology is increasing in the third molar region, the associated chronic oral inflammation has the potential to contribute to a systemic inflammatory response and negative health outcomes. This study was designed to assess the changes in periodontal PD over time in the third molar region, the distal of second molars, or around third molars, as a clinical indication of worsening periodontal pathology in subjects retaining asymptomatic third molars.
Subjects and Methods The data for these analyses are part of a study of subjects with 4 asymptomatic third molars with adjacent second molars, enrolled in an institutional review board-approved longitudinal trial at 2 academic clinical centers, the University of Kentucky and the University of North Carolina. Inclusion criteria for the trial dictated that subjects be healthy (ASA I, II), be between the ages of 14 and 45 years, and have 4 asymptomatic third molars with adjacent second molars. Subjects with the most severe form of periodontal disease (AAP IV), or who had taken antibiotics within 3 months before possible enrollment were excluded from participation. Subjects were enrolled over a 4-year period ending in 2002. Demographic data and data assessing oral health were collected from each subject at baseline and at follow-up exams. After data collection, enrolled subjects had a dental prophylaxis at baseline and at each follow-up exam. To be included in these analyses, subjects had to have had at least 2 follow-up exams after baseline. This assured a minimal level of periodontal care for all subjects in the study. Panoramic radiographs were analyzed for third molar angulation as compared with the long axis of the second molar (mesial/horizontal ⱖ25° or vertical/dis-
PERIODONTAL DISEASE IN SECOND/THIRD MOLAR REGION
tal) and eruption to the occlusal plane or not. Full mouth periodontal probing, 6 sites each tooth, was conducted as a measure of clinical periodontal status at baseline and follow-up. Because third molar periodontal pathology would directly affect this anatomic region of the mouth, periodontal PD in the third molar region, the distal of second molars (2 PD) or around third molars (6 PD), was the focus of these analyses. All second molars could be probed. A third molar that could not be probed because the tooth did not communicate with the oral cavity was coded as unscored. In 53 subjects (20%) all third molars could not be probed at baseline. For all subjects 39% of the third molars (392 of the possible 1,016) could not be probed at baseline. Whether PD around these impacted teeth was possible at follow-up or not, the third molars that could not be probed at baseline were not included in the analyses of change at follow-up. The maximum PD of all second and third molars were aggregated to the subject level: at baseline, subjects were categorized as those who had at least 1 second or third molar with a PD ⱖ4 mm indicating periodontal pathology and those with all teeth ⬍ 4 mm PD. For change from baseline, subjects were categorized as those who had at least 1 tooth with an increase of PD ⱖ2 mm and those who had no teeth exhibiting a 2 mm or greater change in PD. The change in PD of at least 2 mm in the third molar region over time was considered primary because this level of change is considered clinically as an indicator of worsening periodontal disease and accompanying increased oral inflammation. Demographic characteristics and the baseline categorization were compared for subjects with and without changes in PD of at least 2 mm between baseline and follow-up using the Cochran-Mantel-Haenzsel mean row statistic. Level of significance was set at 0.05.
Results Two hundred fifty-four subjects of the 329 described by Blakey et al1 had at least 2 follow-up visits as of May 2005 (Table 1). The majority were female (56%) and Caucasian (80%). African American subjects (13%) were similar in percentages to the US population, but Asian and Hispanic subjects were under-represented. The subjects were well educated (93%) with at least a high school education. Slightly more than half of the subjects were older than 25 years at enrollment. Median follow-up from enrollment to second follow-up visit was 2.2 years (interquartile range 2.0, 2.6 years). At baseline 61% of third molars were at the occlusal plane; 85% were vertical or distoangular.
191
BLAKEY ET AL
Table 1. DEMOGRAPHIC CHARACTERISTICS OF SUBJECTS AT ENROLLMENT (N ⴝ 254) WITH AT LEAST 2 FOLLOW-UP DATA COLLECTION VISITS
Subjects n (%) Female Caucasian African American Other Education at least grade 12 Age ⬍25 years ⱖ25 years Mean age in years (SD) Median follow-up in years IQ
142 (56) 203 (80) 33 (13) 18 (7) 237 (93) 117 (46) 137 (54) 27.5 (7.8) 2.2 2.0, 2.6
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
At baseline, 59% of the subjects had at least 1 PD ⱖ4 mm in the third molar region, a quarter at least 1 PD ⱖ5 mm (Table 2). Forty-one percent of the subjects had at least 1 PD ⱖ4 mm on the distal of the second molar, while 61% of the subjects had a PD ⱖ4 mm around a third molar (Table 2). At the tooth level, mandibular second molars were more likely to have at least 1 PD ⱖ4 mm than maxillary second molars (29% vs 9%), and mandibular third molars more likely than maxillary third molars (53% vs 16%) (data not displayed).
Table 2. FREQUENCIES FOR SUBJECTS WHOSE MAXIMUM PERIODONTAL PROBING DEPTHS AT ENROLLMENT IN THE THIRD MOLAR REGION WERE <4 mm OR >4 mm
Subject-Level Baseline Probing Depth Distal of second molar or third molar ⬍ 4 mm 4 mm 5 mm ⱖ 6 mm ⱖ 4 mm ⱖ 5 mm Distal of second molar ⬍ 4 mm 4 mm 5 mm ⱖ 6 mm ⱖ 4 mm ⱖ 5 mm Third molar ⬍ 4 mm 4 mm 5 mm ⱖ 6 mm ⱖ 4 mm ⱖ 5 mm
Subjects n (%) 103 (40) 86 (34) 38 (15) 27 (11) 151 (59) 65 (26) 151 (59) 61 (24) 24 (9) 18 (7) 103 (41) 42 (17) 78 (39) 73 (36) 35 (17) 16 (8) 124 (61) 51 (8)
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
Table 3. FREQUENCIES OF SUBJECTS WHO EXHIBITED AT LEAST A 2 mm PD INCREASE AT FOLLOW-UP ACCORDING TO THEIR CLASSIFICATION AT BASELINE OF MAXIMUM PERIODONTAL PROBING DEPTHS IN THE THIRD MOLAR REGION (<4 mm VS >4 mm)
Subject-Level Baseline Probing Depth
Subject-Level Change in Probing Depth of at least 2 mm at Follow-Up n (%)
⬍ 4 mm n ⫽ 103 ⱖ 4 mm* n ⫽ 151 Total n ⫽ 254
3 (3) 58 (38) 61 (24)
*Changes in probing depth more likely if at least 1 periodontal probing depth in the third molar region ⱖ4 mm (P ⬍ .001). Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
Twenty-four percent of the subjects had the maximum PD on at least 1 tooth in the third molar region increase by ⱖ2 mm at follow-up (Table 3). If subjects had at least 1 PD ⱖ4 mm at baseline, 38% of these had at least 1 PD deepen by 2 mm or more at follow-up. Only 3% of those with all teeth in the third molar region with ⬍4 mm PD at baseline exhibited the same extent of change (P ⬍ .001). Although not statistically significant, those at least 25 years old at enrollment were more likely to have at least 1 increased PD ⱖ2 mm at follow-up (27% vs 20%) (Table 4). Males were more likely than females (28% vs 20%) and African American subjects were more likely than non-African Americans to have at least 1 increased PD ⱖ2 mm at follow-up (30% vs 23%). If the maxilla and mandible are considered separately because the anatomy in the third molar region differs between jaws, the pattern of PD change ⱖ2 mm persisted. The overall rate for teeth for an increased PD ranged from 5% (maxillary second molar) to 12% (mandibular third molar) (Tables 5, 6). However, increased PD ⱖ2 mm was limited almost always to those teeth with PD ⱖ4 mm at baseline. In the maxilla almost half of the second molars with a deep pocket at baseline had increased PD ⱖ2 mm, more than 31% around a third molar. Of those with a PD ⱖ4 mm at baseline in the mandible, an increased PD ⱖ2 mm was more likely on the distal of a second molar (34%) than around a third molar (23%). If maxillary third molars were erupted to the occlusal plane, a change in PD ⱖ2 mm was more likely than if the third molars were below the occlusal plane (9% vs 3%). A similar pattern existed for mandibular third molars; a change in PD ⱖ2 mm was more likely if the third molars were at the occlusal plane (15% vs 11%) (data not displayed).
192
PERIODONTAL DISEASE IN SECOND/THIRD MOLAR REGION
Table 4. COMPARISON OF DEMOGRAPHIC CHARACTERISTICS OF SUBJECTS WHO DID NOT EXHIBIT A CHANGE IN MAXIMUM PD OF 2 mm IN THE THIRD MOLAR REGION AND THOSE WHO EXHIBITED A CHANGE OF >2 mm
Change in Probing Depth ⬍2 mm n (%) ⱖ2 mm n (%) Age in years ⬍25 yr ⱖ25 yr Female Male African American Non-African American
94 (80) 99 (72) 113 (80) 81 (72) 23 (70) 171 (77)
P Value
23 (20) 38 (27) 29 (20) 32 (28) 10 (30) 51 (23)
.13 .14 .36
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
Discussion Our analyses add weight to Blakey et al’s conclusions that periodontal pathology is more common in the third molar region than clinicians expected.1 Almost two thirds of the asymptomatic subjects had at least 1 PD ⱖ4 mm. If the third molars had a communication to the oral cavity and could be probed, a PD ⱖ4 mm was more likely around third molars (61%) but the distal of second molars was affected in 41%. The most important finding from our study was that 38% of the subjects with PD ⱖ4 mm at enrollment had clinical evidence that their periodontal condition had worsened in a relatively short time,
Table 5. PERIODONTAL PROBING DEPTHS AT BASELINE IN THE MAXILLARY THIRD MOLAR REGION BY CHANGES IN PERIODONTAL PROBING DEPTH OF AT LEAST 2 mm
Tooth-Level Baseline Probing Depth Distal of second molar* ⬍ 4 mm n ⫽ 459 ⱖ 4 mm n ⫽ 48 Total n ⫽ 507 Third molar† ⬍ 4 mm n ⫽ 264 ⱖ 4 mm n ⫽ 51 Total n ⫽ 315
Tooth-Level Change in Probing Depth of at least 2 mm at Follow-Up n (%) 3 (1) 23 (48) 26 (5) 2 (1) 16 (31) 18 (6)
with a median follow-up of 2.2 years. Despite anatomic differences between jaws, the pattern of the PD change ⱖ2 mm, occurring almost always with a prior PD ⱖ4 mm, persisted if maxillary or mandibular second or third molar PD was considered separately. Two thirds of all third molars in our study subjects were erupted to the occlusal plane at enrollment. However, the erupted third molars were just as likely to have a change in PD as third molars below the occlusal plane. These findings are counter to the expectations of the public and many clinicians, who expect more periodontal pathology with impacted third molars and fewer with erupted third molars.
Table 6. PERIODONTAL PROBING DEPTHS AT BASELINE IN THE MANDIBULAR THIRD MOLAR REGION BY CHANGES IN PERIODONTAL PROBING DEPTH OF AT LEAST 2 mm
Tooth-Level Baseline Probing Depth Distal of second molar ⬍ 4 mm n ⫽ 360 ⱖ 4 mm n ⫽ 148 Total n ⫽ 508 Third molar† ⬍ 4 mm n ⫽ 148 ⱖ 4 mm n ⫽ 165 Total n ⫽ 313
Tooth-Level Change in Probing Depth at least 2 mm at Follow-Up* n (%) 1 (⬍1) 51 (34) 52 (10) 0 (0) 38 (23) 38 (12)
*Data missing for 3 teeth. †For 195 impacted teeth the third molars could not be probed at baseline.
*Data missing for 2 teeth. †For 197 impacted teeth the third molars could not be probed at baseline.
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
193
BLAKEY ET AL
What are the clinical implications of our analyses? Our data suggest that clinical findings of a PD ⱖ4 mm in the third molar region without symptoms may not be benign. White et al2,3 have documented that even in subjects with a relatively young median age of 28 years, increased PD is accompanied by high levels of periodontal pathogens and gingival crevicular fluid inflammatory mediators. Further analysis is planned for our study subjects at follow-up, but the finding of increasing PD would be expected to be accompanied by increasing levels of periodontal pathogens and inflammatory mediators, both additional risk markers for chronic oral inflammation. A systemic response to the chronic oral inflammation might follow. Because of the bony architecture and the usual poor quality of soft tissue in the third molar region, periodontal problems are difficult to treat or eradicate. Most dentists would recommend removal of the periodontally involved third molar as the most effective definitive treatment. If a patient decides to retain a periodontally involved third molar, he or she is committed to a lifetime of aggressive treatment to prevent the chronic inflammatory condition from worsening. Our data also suggest that periodontal probing may be an important clinical tool for detecting and assessing periodontal pathology over time on the distal of second molars or around third molars. For retained third molars, clinical assessment by periodontal prob-
ing may prove to a sufficient clinical monitoring procedure for both erupted and impacted third molars. Acknowledgements The authors thank Debora Price for assistance in managing data for this project and Sharon Williams, Robin Hambly, Donna Mischel, Charlotte Stokley, and Tiffany Hambright for their assistance as clinical coordinators.
References 1. Blakey GH, Marciani RD, Haug RH, et al: Periodontal pathology associated with asymptomatic third molars. J Oral Maxillofac Surg 60:1227, 2002 2. White RP Jr, Madianos PN, Offenbacher S, et al: Microbial complexes detected in the second/third molar region in subjects with asymptomatic third molars. J Oral Maxillofac Surg 60:1234, 2002 3. White RP Jr, Offenbacher S, Haug RH, et al: Inflammatory mediators and periodontitis in subjects with asymptomatic third molars. J Oral Maxillofac Surg 60:1241, 2002 4. Hansson GK: Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352:1685, 2005 5. Offenbacher S, Lieff S, Boggess KA, et al: Maternal periodontitis and prematurity. Part I: Obstetric outcome of prematurity and growth restriction. Ann Periodontol 6:164, 2001 6. Slade GD, Ghezzi EM, Heiss G, et al: Relationship between periodontal disease and C-reactive protein among adults in the Atherosclerosis Risk in Communities study. Arch Intern Med 163:1172, 2003 7. Elter JR, Champagne CM, Offenbacher S, et al: Relationship of periodontal disease and tooth loss to prevalence of coronary disease. J Periodontol 75:782, 2004 8. Kshirsagar AV, Moss KL, Elter JR, et al: Periodontal disease is associated with renal insufficiency in the Atherosclerosis Risk In Communities (ARIC) study. Am J Kidney Dis 45:650, 2005
Progression of Periodontal Disease in the Second/Third Molar Region in Subjects With Asymptomatic Third Molars George H. Blakey, DDS,* M. Thomas Jacks, DDS,† Steven Offenbacher, DDS, PhD,‡ Paige E. Nance, DDS,§ Ceib Phillips, PhD,储 Richard H. Haug, DDS,¶ and Raymond P. White, Jr, DDS, PhD# Purpose: To assess the change in periodontal status over time by periodontal probing depth (PD) in the
third molar region. Subjects and Methods: The data for these analyses are part of a study of subjects enrolled with 4
asymptomatic third molars with adjacent second molars in an institutional review board-approved longitudinal trial. Full mouth periodontal probing was conducted to determine periodontal status at baseline and follow-up. Panoramic radiographs were analyzed for angulation and degree of eruption of third molars. Subjects were categorized as those who exhibited at least a 2 mm change in periodontal PD between baseline and follow-up in the third molar region, the distal of a second molar or around a third molar, and those who did not exhibit a 2 mm or greater change. Subjects with and without changes in PD were compared with Cochran-Mantel-Haenzsel statistics. Level of significance was set at 0.05. Results: Data from 254 subjects with at least 2 annual follow-up visits were available for analysis. Mean age at baseline was 27.5 years. Median follow-up from baseline to the second follow-up visit was 2.2 years (interquartile range 2.0, 2.6). At enrollment, 59% of the subjects had at least 1 PD ⱖ4 mm in the third molar region, one quarter had a PD ⱖ5 mm. Twenty-four percent of the subjects had at least 1 tooth that had an increased PD ⱖ2 mm in the third molar region at follow-up. If subjects had at least 1 PD ⱖ4 mm at baseline, 38% had at least 1 PD deepen by 2 mm or more at follow-up. Only 3% of those who had all teeth with a PD of less than 4 mm at baseline exhibited a change of ⱖ2 mm (P ⬍ .001). Conclusion: Increased periodontal PDs ⱖ2 mm were often found in the third molar region for asymptomatic subjects with at least 1 PD ⱖ4 mm at enrollment, clinical measures that indicated increased periodontal pathology, and a deteriorating periodontal condition. © 2006 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg 64:189-193, 2006 Blakey et al1 reported a higher prevalence of increased periodontal probing depths (PD) in the third molar region than clinicians expected. At baseline, 25% of the sample of 329 subjects enrolled in a longitudinal trial had at least 1 PD ⱖ5 mm in the third
molar region; one third of subjects at least 25 years of age had at least 1 PD ⱖ5 mm. Only 4 subjects had PD ⱖ5 mm anterior to the third molar region. White et al2,3 documented that the same subjects who had a PD ⱖ5 mm at baseline had elevated levels
*Clinical Assistant Professor, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. †Former Senior Resident, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. ‡Ora Pharma Professor, Department of Periodontics, School of Dentistry, University of North Carolina, Chapel Hill, NC. §Clinical Research Fellow, Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. 储Professor, Department of Orthodontics, School of Dentistry, University of North Carolina, Chapel Hill, NC. ¶Professor, Department of Oral and Maxillofacial Surgery, Assistant Dean, College of Dentistry, University of Kentucky, Lexington, KY.
#Dalton L. McMichael Professor, Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC. Supported in part by the Oral and Maxillofacial Surgery Foundation, American Association of Oral and Maxillofacial Surgeons, and the Dental Foundation of North Carolina. Address correspondence and reprint requests to Dr White: Department of Oral and Maxillofacial Surgery, School of Dentistry, University of North Carolina, Chapel Hill, NC 27599-7450; e-mail: [email protected] © 2006 American Association of Oral and Maxillofacial Surgeons
0278-2391/06/6402-0007$32.00/0 doi:10.1016/j.joms.2005.10.014
189
190 of “orange” and “red” complex periodontal pathogens detected in biofilm samples from the distal of second molars and elevated levels of the gingival crevicular fluid inflammatory mediator, IL-1. These data suggest that retained third molars with periodontal pathology are a source of chronic oral inflammation. Current clinical research continues to focus on the impact of chronic inflammation at remote anatomic sites with cardiovascular disease.4 Chronic oral inflammation associated with periodontal disease has been implicated in increasing the risk for cardiovascular disease as well as for renal insufficiency and preterm birth.5-8 The common denominator for all of these clinical conditions is endothelial cell activation associated with chronic inflammation at remote sites including the oral cavity. Increased PD over time is a clinical measure of an increase in severity of periodontal disease and an increased level of chronic oral inflammation. If periodontal pathology is increasing in the third molar region, the associated chronic oral inflammation has the potential to contribute to a systemic inflammatory response and negative health outcomes. This study was designed to assess the changes in periodontal PD over time in the third molar region, the distal of second molars, or around third molars, as a clinical indication of worsening periodontal pathology in subjects retaining asymptomatic third molars.
Subjects and Methods The data for these analyses are part of a study of subjects with 4 asymptomatic third molars with adjacent second molars, enrolled in an institutional review board-approved longitudinal trial at 2 academic clinical centers, the University of Kentucky and the University of North Carolina. Inclusion criteria for the trial dictated that subjects be healthy (ASA I, II), be between the ages of 14 and 45 years, and have 4 asymptomatic third molars with adjacent second molars. Subjects with the most severe form of periodontal disease (AAP IV), or who had taken antibiotics within 3 months before possible enrollment were excluded from participation. Subjects were enrolled over a 4-year period ending in 2002. Demographic data and data assessing oral health were collected from each subject at baseline and at follow-up exams. After data collection, enrolled subjects had a dental prophylaxis at baseline and at each follow-up exam. To be included in these analyses, subjects had to have had at least 2 follow-up exams after baseline. This assured a minimal level of periodontal care for all subjects in the study. Panoramic radiographs were analyzed for third molar angulation as compared with the long axis of the second molar (mesial/horizontal ⱖ25° or vertical/dis-
PERIODONTAL DISEASE IN SECOND/THIRD MOLAR REGION
tal) and eruption to the occlusal plane or not. Full mouth periodontal probing, 6 sites each tooth, was conducted as a measure of clinical periodontal status at baseline and follow-up. Because third molar periodontal pathology would directly affect this anatomic region of the mouth, periodontal PD in the third molar region, the distal of second molars (2 PD) or around third molars (6 PD), was the focus of these analyses. All second molars could be probed. A third molar that could not be probed because the tooth did not communicate with the oral cavity was coded as unscored. In 53 subjects (20%) all third molars could not be probed at baseline. For all subjects 39% of the third molars (392 of the possible 1,016) could not be probed at baseline. Whether PD around these impacted teeth was possible at follow-up or not, the third molars that could not be probed at baseline were not included in the analyses of change at follow-up. The maximum PD of all second and third molars were aggregated to the subject level: at baseline, subjects were categorized as those who had at least 1 second or third molar with a PD ⱖ4 mm indicating periodontal pathology and those with all teeth ⬍ 4 mm PD. For change from baseline, subjects were categorized as those who had at least 1 tooth with an increase of PD ⱖ2 mm and those who had no teeth exhibiting a 2 mm or greater change in PD. The change in PD of at least 2 mm in the third molar region over time was considered primary because this level of change is considered clinically as an indicator of worsening periodontal disease and accompanying increased oral inflammation. Demographic characteristics and the baseline categorization were compared for subjects with and without changes in PD of at least 2 mm between baseline and follow-up using the Cochran-Mantel-Haenzsel mean row statistic. Level of significance was set at 0.05.
Results Two hundred fifty-four subjects of the 329 described by Blakey et al1 had at least 2 follow-up visits as of May 2005 (Table 1). The majority were female (56%) and Caucasian (80%). African American subjects (13%) were similar in percentages to the US population, but Asian and Hispanic subjects were under-represented. The subjects were well educated (93%) with at least a high school education. Slightly more than half of the subjects were older than 25 years at enrollment. Median follow-up from enrollment to second follow-up visit was 2.2 years (interquartile range 2.0, 2.6 years). At baseline 61% of third molars were at the occlusal plane; 85% were vertical or distoangular.
191
BLAKEY ET AL
Table 1. DEMOGRAPHIC CHARACTERISTICS OF SUBJECTS AT ENROLLMENT (N ⴝ 254) WITH AT LEAST 2 FOLLOW-UP DATA COLLECTION VISITS
Subjects n (%) Female Caucasian African American Other Education at least grade 12 Age ⬍25 years ⱖ25 years Mean age in years (SD) Median follow-up in years IQ
142 (56) 203 (80) 33 (13) 18 (7) 237 (93) 117 (46) 137 (54) 27.5 (7.8) 2.2 2.0, 2.6
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
At baseline, 59% of the subjects had at least 1 PD ⱖ4 mm in the third molar region, a quarter at least 1 PD ⱖ5 mm (Table 2). Forty-one percent of the subjects had at least 1 PD ⱖ4 mm on the distal of the second molar, while 61% of the subjects had a PD ⱖ4 mm around a third molar (Table 2). At the tooth level, mandibular second molars were more likely to have at least 1 PD ⱖ4 mm than maxillary second molars (29% vs 9%), and mandibular third molars more likely than maxillary third molars (53% vs 16%) (data not displayed).
Table 2. FREQUENCIES FOR SUBJECTS WHOSE MAXIMUM PERIODONTAL PROBING DEPTHS AT ENROLLMENT IN THE THIRD MOLAR REGION WERE <4 mm OR >4 mm
Subject-Level Baseline Probing Depth Distal of second molar or third molar ⬍ 4 mm 4 mm 5 mm ⱖ 6 mm ⱖ 4 mm ⱖ 5 mm Distal of second molar ⬍ 4 mm 4 mm 5 mm ⱖ 6 mm ⱖ 4 mm ⱖ 5 mm Third molar ⬍ 4 mm 4 mm 5 mm ⱖ 6 mm ⱖ 4 mm ⱖ 5 mm
Subjects n (%) 103 (40) 86 (34) 38 (15) 27 (11) 151 (59) 65 (26) 151 (59) 61 (24) 24 (9) 18 (7) 103 (41) 42 (17) 78 (39) 73 (36) 35 (17) 16 (8) 124 (61) 51 (8)
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
Table 3. FREQUENCIES OF SUBJECTS WHO EXHIBITED AT LEAST A 2 mm PD INCREASE AT FOLLOW-UP ACCORDING TO THEIR CLASSIFICATION AT BASELINE OF MAXIMUM PERIODONTAL PROBING DEPTHS IN THE THIRD MOLAR REGION (<4 mm VS >4 mm)
Subject-Level Baseline Probing Depth
Subject-Level Change in Probing Depth of at least 2 mm at Follow-Up n (%)
⬍ 4 mm n ⫽ 103 ⱖ 4 mm* n ⫽ 151 Total n ⫽ 254
3 (3) 58 (38) 61 (24)
*Changes in probing depth more likely if at least 1 periodontal probing depth in the third molar region ⱖ4 mm (P ⬍ .001). Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
Twenty-four percent of the subjects had the maximum PD on at least 1 tooth in the third molar region increase by ⱖ2 mm at follow-up (Table 3). If subjects had at least 1 PD ⱖ4 mm at baseline, 38% of these had at least 1 PD deepen by 2 mm or more at follow-up. Only 3% of those with all teeth in the third molar region with ⬍4 mm PD at baseline exhibited the same extent of change (P ⬍ .001). Although not statistically significant, those at least 25 years old at enrollment were more likely to have at least 1 increased PD ⱖ2 mm at follow-up (27% vs 20%) (Table 4). Males were more likely than females (28% vs 20%) and African American subjects were more likely than non-African Americans to have at least 1 increased PD ⱖ2 mm at follow-up (30% vs 23%). If the maxilla and mandible are considered separately because the anatomy in the third molar region differs between jaws, the pattern of PD change ⱖ2 mm persisted. The overall rate for teeth for an increased PD ranged from 5% (maxillary second molar) to 12% (mandibular third molar) (Tables 5, 6). However, increased PD ⱖ2 mm was limited almost always to those teeth with PD ⱖ4 mm at baseline. In the maxilla almost half of the second molars with a deep pocket at baseline had increased PD ⱖ2 mm, more than 31% around a third molar. Of those with a PD ⱖ4 mm at baseline in the mandible, an increased PD ⱖ2 mm was more likely on the distal of a second molar (34%) than around a third molar (23%). If maxillary third molars were erupted to the occlusal plane, a change in PD ⱖ2 mm was more likely than if the third molars were below the occlusal plane (9% vs 3%). A similar pattern existed for mandibular third molars; a change in PD ⱖ2 mm was more likely if the third molars were at the occlusal plane (15% vs 11%) (data not displayed).
192
PERIODONTAL DISEASE IN SECOND/THIRD MOLAR REGION
Table 4. COMPARISON OF DEMOGRAPHIC CHARACTERISTICS OF SUBJECTS WHO DID NOT EXHIBIT A CHANGE IN MAXIMUM PD OF 2 mm IN THE THIRD MOLAR REGION AND THOSE WHO EXHIBITED A CHANGE OF >2 mm
Change in Probing Depth ⬍2 mm n (%) ⱖ2 mm n (%) Age in years ⬍25 yr ⱖ25 yr Female Male African American Non-African American
94 (80) 99 (72) 113 (80) 81 (72) 23 (70) 171 (77)
P Value
23 (20) 38 (27) 29 (20) 32 (28) 10 (30) 51 (23)
.13 .14 .36
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
Discussion Our analyses add weight to Blakey et al’s conclusions that periodontal pathology is more common in the third molar region than clinicians expected.1 Almost two thirds of the asymptomatic subjects had at least 1 PD ⱖ4 mm. If the third molars had a communication to the oral cavity and could be probed, a PD ⱖ4 mm was more likely around third molars (61%) but the distal of second molars was affected in 41%. The most important finding from our study was that 38% of the subjects with PD ⱖ4 mm at enrollment had clinical evidence that their periodontal condition had worsened in a relatively short time,
Table 5. PERIODONTAL PROBING DEPTHS AT BASELINE IN THE MAXILLARY THIRD MOLAR REGION BY CHANGES IN PERIODONTAL PROBING DEPTH OF AT LEAST 2 mm
Tooth-Level Baseline Probing Depth Distal of second molar* ⬍ 4 mm n ⫽ 459 ⱖ 4 mm n ⫽ 48 Total n ⫽ 507 Third molar† ⬍ 4 mm n ⫽ 264 ⱖ 4 mm n ⫽ 51 Total n ⫽ 315
Tooth-Level Change in Probing Depth of at least 2 mm at Follow-Up n (%) 3 (1) 23 (48) 26 (5) 2 (1) 16 (31) 18 (6)
with a median follow-up of 2.2 years. Despite anatomic differences between jaws, the pattern of the PD change ⱖ2 mm, occurring almost always with a prior PD ⱖ4 mm, persisted if maxillary or mandibular second or third molar PD was considered separately. Two thirds of all third molars in our study subjects were erupted to the occlusal plane at enrollment. However, the erupted third molars were just as likely to have a change in PD as third molars below the occlusal plane. These findings are counter to the expectations of the public and many clinicians, who expect more periodontal pathology with impacted third molars and fewer with erupted third molars.
Table 6. PERIODONTAL PROBING DEPTHS AT BASELINE IN THE MANDIBULAR THIRD MOLAR REGION BY CHANGES IN PERIODONTAL PROBING DEPTH OF AT LEAST 2 mm
Tooth-Level Baseline Probing Depth Distal of second molar ⬍ 4 mm n ⫽ 360 ⱖ 4 mm n ⫽ 148 Total n ⫽ 508 Third molar† ⬍ 4 mm n ⫽ 148 ⱖ 4 mm n ⫽ 165 Total n ⫽ 313
Tooth-Level Change in Probing Depth at least 2 mm at Follow-Up* n (%) 1 (⬍1) 51 (34) 52 (10) 0 (0) 38 (23) 38 (12)
*Data missing for 3 teeth. †For 195 impacted teeth the third molars could not be probed at baseline.
*Data missing for 2 teeth. †For 197 impacted teeth the third molars could not be probed at baseline.
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
Blakey et al. Periodontal Disease in Second/Third Molar Region. J Oral Maxillofac Surg 2006.
193
BLAKEY ET AL
What are the clinical implications of our analyses? Our data suggest that clinical findings of a PD ⱖ4 mm in the third molar region without symptoms may not be benign. White et al2,3 have documented that even in subjects with a relatively young median age of 28 years, increased PD is accompanied by high levels of periodontal pathogens and gingival crevicular fluid inflammatory mediators. Further analysis is planned for our study subjects at follow-up, but the finding of increasing PD would be expected to be accompanied by increasing levels of periodontal pathogens and inflammatory mediators, both additional risk markers for chronic oral inflammation. A systemic response to the chronic oral inflammation might follow. Because of the bony architecture and the usual poor quality of soft tissue in the third molar region, periodontal problems are difficult to treat or eradicate. Most dentists would recommend removal of the periodontally involved third molar as the most effective definitive treatment. If a patient decides to retain a periodontally involved third molar, he or she is committed to a lifetime of aggressive treatment to prevent the chronic inflammatory condition from worsening. Our data also suggest that periodontal probing may be an important clinical tool for detecting and assessing periodontal pathology over time on the distal of second molars or around third molars. For retained third molars, clinical assessment by periodontal prob-
ing may prove to a sufficient clinical monitoring procedure for both erupted and impacted third molars. Acknowledgements The authors thank Debora Price for assistance in managing data for this project and Sharon Williams, Robin Hambly, Donna Mischel, Charlotte Stokley, and Tiffany Hambright for their assistance as clinical coordinators.
References 1. Blakey GH, Marciani RD, Haug RH, et al: Periodontal pathology associated with asymptomatic third molars. J Oral Maxillofac Surg 60:1227, 2002 2. White RP Jr, Madianos PN, Offenbacher S, et al: Microbial complexes detected in the second/third molar region in subjects with asymptomatic third molars. J Oral Maxillofac Surg 60:1234, 2002 3. White RP Jr, Offenbacher S, Haug RH, et al: Inflammatory mediators and periodontitis in subjects with asymptomatic third molars. J Oral Maxillofac Surg 60:1241, 2002 4. Hansson GK: Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 352:1685, 2005 5. Offenbacher S, Lieff S, Boggess KA, et al: Maternal periodontitis and prematurity. Part I: Obstetric outcome of prematurity and growth restriction. Ann Periodontol 6:164, 2001 6. Slade GD, Ghezzi EM, Heiss G, et al: Relationship between periodontal disease and C-reactive protein among adults in the Atherosclerosis Risk in Communities study. Arch Intern Med 163:1172, 2003 7. Elter JR, Champagne CM, Offenbacher S, et al: Relationship of periodontal disease and tooth loss to prevalence of coronary disease. J Periodontol 75:782, 2004 8. Kshirsagar AV, Moss KL, Elter JR, et al: Periodontal disease is associated with renal insufficiency in the Atherosclerosis Risk In Communities (ARIC) study. Am J Kidney Dis 45:650, 2005