Radiographic Position of Impacted Mandibular Third Molars and Their Association with Pathological Conditions

Objectives This study aimed to assess the radiographic position of impacted mandibular third molars (IMTMs) and their association with pathological conditions. Materials and Methods The impaction depth, relationship with ramus, and angulation of 1600 IMTMs and their association with 2nd molar distal caries and root resorption, pathological conditions, and proximity to the mandibular canal were evaluated on panoramic radiographs. The IMTM position was determined based on the depth of impaction according to the Pell and Gregory classification, relationship with ramus according to the Pell and Gregory classification, and angulation according to the Winter's classification. The classical and Bayesian logistic regressions were applied to analyze the effect of IMTM position on the associated complications using the odds ratio (OR) and 95% confidence interval (credible interval for Bayesian models). Two-tailed P value < 0.05 was considered statistically significant. Results Of 1600 IMTMs evaluated in this study, 195 (12.2%), 252 (15.8%), and 119 (7.4%) had caused second molar distal caries, second molar root resorption, and pathological lesions, respectively, and 872 (54.5%) had contact with the mandibular canal. Impaction angulation was a risk factor for second molar distal caries (maximum OR = 5.01, 95% CI: 3.12–8.18). Changed angulation and greater impaction depth were the risk factors for second molar root resorption (minimum OR = 1.64, 95% CI: 0.58–4.02). Decreased distance between the ramus and distal side of the second molar was a risk factor for associated pathological lesions (minimum OR = 2.73, 95% CI: 1.79–4.25). Mesioangular and horizontal angulations and greater impaction depth were the risk factors for contact with the mandibular canal (maximum OR = 3.44, 95% CI: 2.6–4.57 and minimum OR = 1.3, 95% CI: 094–1.8). Conclusions The frequency of complications associated with IMTMs was low, but considerable. The occurrence of these conditions might be affected by the impaction position. Thus, regular follow-ups are recommended in order to be able to surgically intervene when the first signs of pathologies arise.

ird molar surgery is among the most common surgical procedures worldwide. is surgical procedure may be indicated for the following purposes: (I) to treat the symptomatic pathologies related to impaction, (II) to prevent future pathological conditions, or (III) for non-pathological reasons, e.g., prior to orthognathic surgery, orthodontic treatment, and removable denture treatment [14]. Despite the necessity of removal of impacted third molars in the abovementioned situations, their preventive removal is still a matter of controversy.
Hundreds of patients undergo third molar surgery every year. However, the real benefit of this procedure is still a matter of debate, and the advantages and disadvantages of prophylactic third molar tooth removal should be weighed against the treatment of subsequent complications in case of their development. In this respect, various strategies have been adopted by different countries. Preventive removal has been rejected in the UK by the National Institute of Clinical Excellence [15], while there is controversy in the United States on this topic between the American Association of Oral and Maxillofacial Surgeons (AAOMS) and the American Public Health Association (APHA). AAOMS believes in encouraging prophylactic removal of third molars in young ages to prevent future problems and to ensure optimal healing. On the other hand, APHA disagrees with the prophylactic removal of third molars, because of its unnecessary costs for patients and the society, avoidable morbidity, and the risks of permanent injury [16,17]. Moreover, in Germany and Japan, third molars are removed if their physiological eruption is not expected [18,19]. us, a general consensus is lacking on this topic.
Although the National Institute of Clinical Excellence, AAOMS, and APHA have published guidelines for management of impacted third molars, AAOMS calls for further studies to determine the prevalence of pathological conditions associated with impacted third molars [20].
It appears that information about the pathological conditions associated with third molar impaction plays a key role in compiling a comprehensive guideline regarding third molar management. Hence, the aim of this study was to radiographically evaluate the impaction status of impacted mandibular third molars (impaction depth, relation with the ascending ramus, and angulation) and the associated pathological conditions.

Study Design/Sample.
To address the research question, a retrospective cross-sectional study was conducted on panoramic radiographs of patients referred to a private oral and maxillofacial radiology clinic in Qazvin city, Iran.
At the onset of the study, in order to calibrate the examiners for data collection and to enhance data recording, a checklist was designed under the supervision of an oral and maxillofacial surgeon with 20 years of clinical experience ( Figure 1). e examiners included an oral and maxillofacial radiologist with 10 years of clinical experience, and a senior dental student.
High-quality digital panoramic radiographs of patients were retrieved from the archives. e images had been obtained by Cranex 3D x-ray system (Soredex, Finland) with the standard exposure parameters of 70 kVp, 16 mA, and 15 s. e magnification rate ranged from 0% to 50%. e radiographs were selected by convenience sampling. Patients were excluded if they met any of the following conditions: age under 20 years (since the eruption of third molars usually starts at this age) [21], previous history of trauma to the jaw involving the dentition, craniofacial anomalies (for example, Down syndrome), mandibular third molars with incomplete root formation, erupted mandibular third molars, mandibular third molars with less than half of their distal cusp in the ascending ramus, missing mandibular third molars, missing mandibular second molars, and missing mandibular first molars resulting in tilting of the adjacent mandibular second molar.

Study
Variables. Independent variables evaluated in this study were depth of impaction classified according to the Pell and Gregory classification (Figure 2), relation with the ramus classified according to the Pell and Gregory classification ( Figure 3) [22], and angulation of IMTMs according to the Winter's classification ( Figure 4) [23]. e longitudinal axis of mandibular molars was determined as the line connecting the midpoint of the occlusal surface and bifurcation of the tooth. e angle formed between the longitudinal axis of the second and third molars was measured by an orthodontic protractor ( Figure 5).
Dependent variables evaluated in this study were presence of caries in the distal surface of the adjacent second molar, root resorption of the second molar, proximity to the mandibular canal, and presence of intra-bony pathological lesions related to the IMTM.
In order to distinguish distal caries from distal root resorption, discontinuity and irregularity of the root surface and loss of tooth structure at the cervical region, lateral wall, or apex was considered as root resorption [24], while a distal radiolucency with relation to the oral environment and a gap between the third and second molars that caused food impaction indicated the presence of distal caries [4].
Proximity to the mandibular canal was assessed by using the Rood and Shehab radiographic markers that indicate close relationship between the IMTM and the mandibular canal ( Figure 6) [25]. According to Meyer's classification for the correlation of third molars with the mandibular canal, "notching of the root" is a condition where the mandibular canal is in close physical contact with an indentation in the lateral side of the root [26]. Accordingly, IMTMs were categorized into three groups of "in contact with the inferior alveolar nerve (IAN)," "no contact with the IAN," and "in contact with the external border of the mandibular canal." In the present study, any radiolucency, e.g., follicular hyperplasia, odontogenic cysts, or tumors related to the IMTMs, or any reduction in bone density around the IMTMs was considered as a pathological lesion [10]. Any radiolucency around the impacted tooth that was larger than 3 mm was considered as a pathological lesion (Figure 7).

Data Collection.
Data were collected over a 9-month period. e images were stored on a hard disk drive and were evaluated in a dark room on a SONY VPCCW laptop computer. e checklist was once filled out by a senior dental student, and then all items were double-checked by a radiologist. If there was any disagreement, both examiners discussed the case with each other until a consensus was reached. erefore, no inter-examiner error was expected. A third molar was considered impacted if it had no functional occlusion with completely formed roots [1]. e radiographs were evaluated anonymously.
e study protocol was approved by the ethics committee of Qazvin University of Medical Sciences (QUMS.REC.1394.30).

Statistical Analysis.
Classical and Bayesian logistic regressions were used to analyze the effects of IMTM position on pathological conditions by using the odds ratio (OR) and 95% confidence interval (credible interval for Bayesian models). Two-tailed P values < 0.05 were considered statistically significant. Statistical analyses were performed using R software (version 4.0.1).

Results
A total of 2018 panoramic radiographs of 2832 teeth were evaluated, out of which 1011 panoramic images were entered in the study. A total of 589 patients had bilateral IMTMs; therefore, 1600 IMTMs of patients between 20 and 55 years (mean age of 25.73 ± 5.26 years) were evaluated. e frequency of mesioangular position (36%) was higher than other positions; moreover, class B (46.8%) and class II (51.3%) were the most frequent impaction positions. Table 1 shows the frequency of different impaction positions Gregory classification with respect to the occlusal plane. Class A: the highest part of the mandibular third molar is located on the same level or above the occlusal plane of the adjacent second molar. Class B: the highest part of the mandibular third molar is located between the occlusal plane and the cervical line of the second molar. Class C: the highest part of the mandibular third molar is located below the cervical line of the second molar. and ramus relation of IMTMs according to the Pell and Gregory classification.
Of 1600 IMTMs evaluated in this study, 872 (54.5%) had contact with the internal space of the mandibular canal, 207 (12.9%) had contact with the mandibular canal borders, and 521 (32.6%) had no contact with the canal. Also, 252 (15.8%) IMTMs had caused second molar root resorption, 195 (12.2%) had caused distal caries in the adjacent second molar, and 119 (7.4%) cases had pathological lesions.
Class A position had the strongest association with second molar caries and pathological lesions. Moreover, class B and class C both had higher correlation with contact with the mandibular canal and distal root resorption (Table 2). A strong relationship existed between the ramus relation (according to the Pell and Gregory classification) and presence of complications (Table 3). Second molar distal caries and root resorption were more frequent in class I position, while IMTM pathological lesions had the highest association with class Ш position (OR � 8.07, 95% CI: 2.76-20.84, P < 0.001) and class III had higher association with contact with the mandibular canal (OR � 1.34, 95% CI: 0.56-3.75, P � 0.535) ( Table 3).
Change in angulation of third molar from the vertical position had the highest correlation with second molar distal root resorption (minimum OR � 1.64, 95% CI: 0.58-4.02, P < 0.305). Second molar distal caries and contact with the mandibular canal had the highest correlation with mesioangular and vertical positions. e least correlation was with pathological lesions (Table 4). Table 5 shows the odds of contact of IMTM root with the mandibular canal border, and interference of the IMTM root

Discussion
is study provided new evidence for the management of IMTMs according to the correlation of impaction position in three dimensions (tooth angulation, Pell and Gregory occlusogingival position, and Pell and Gregory mesiodistal position) and some complications.

Relationship between Distal Caries and IMTM Position.
In the present study, distal caries was observed in 195 (12.2%) second molars out of 1600 teeth investigated. As panoramic radiography may have lower diagnostic accuracy for detection of proximal caries [27], 12.2% rate of second molar distal caries can only be an estimation of the actual prevalence of distal caries, and the frequency rate reported in the present study is probably an underestimation of the actual rate. However, Rushton et al. [28] declared that panoramic radiography is appropriate for detection of clinically evident carious lesions. e incidence of second molar distal caries is reportedly 7%-42.7% in the literature [3,[8][9][10]29]. Variations in the reported rates may be related to the age range of patients, cultural and socioeconomic differences of the study populations, their oral hygiene habits, the diagnostic methods used, and differences in assessing the second molar distal caries in one or both jaws. To the best of the authors' knowledge, the correlation of mandibular third molar impaction position and second molar distal caries and the effect of different positions and angulations have not been adequately studied.
Falci et al. [3] reported that second molar distal caries occurs more frequently in class II, followed by class I and class III IMTMs. In the present study, class I IMTMs exhibited the strongest association with second molar distal caries (62.6%), followed by class II (37.4%) and class III (0%) IMTMs.
is finding indicates that second molar distal caries may be absent when an IMTM is fully embedded in the ramus bone, as there is no contact between the IMTM and the adjacent tooth. Significant differences between class I impaction versus class II and class III impactions reinforce the idea that plaque accumulation and food impaction increase the risk of second molar distal caries.
A strong correlation was found between the impaction depth (Pell and Gregory classification) and second molar distal caries in the present study, since 75.4% of IMTMs causing second molar distal caries had class A impaction, 24.1% had class B impaction, and 1% had class C impaction. By an increase in depth of impaction, risk of second molar caries decreased (OR � 0.24, 95% CI: 0.17-0.34, P < 0.001 for class B and OR � 0.04, 95% CI: 0.01-0.14, P < 0.001 for class C). is finding was in accordance with the findings of other studies [2,3,29]. Plaque accumulation and food impaction have higher frequency in IMTMs with class A position due to their close contact with the second molar. In contrast with the present study, Falci et al. [3] found no significant correlation between impaction depth and distal caries.
Chung et al. [29] found 27 caries-free class C third molars in their study population. ey discussed that a class C third molar is completely impacted and its crown is below the cervical line of the second molar; thus, it cannot cause second molar distal caries. Contrary to the findings of Chung et al. [29], one class C IMTM had caused distal caries in the adjacent tooth in our study.
is particular case was a horizontal IMTM having a contact point with the cementoenamel junction (CEJ) of the adjacent tooth causing an extensive carious lesion starting in the second molar's crown and extending down and involving the coronal third of the distal root. In such cases, the angulation of tooth and the location of contact point must be considered. Ozec et al. [30] reported that a contact point on the CEJ of the second molar had a statistically significant effect on development of distal caries. We also found that tooth angulation had a significant effect on development of distal caries in the adjacent tooth. In our study, 74.4% of all distal caries occurred in presence of mesioangular and horizontal IMTMs, in a decreasing order Figure 7: Any radiolucency around the impacted tooth that was larger than 3 mm was considered as a pathological lesion.

Second Molar Root Resorption and IMTM Position.
Second molar root resorption caused by the pressure applied by the third molar has been explained in different studies [4,8,20,24,31]. e incidence of second molar root resorption is 0.3%-9.5% [4, 6, 8-10, 31, 32]. e highest incidence of second molar root resorption was reported by Nemcovsky et al. [33]. In the present study, the frequency of second molar root resorption was 15.8%, which is considerable. One probable explanation for the variations in the reported frequency rates of root resorption could be the different definitions of root resorption. In some studies, root resorption was defined as a clear loss of root structure of the adjacent second molar [4,6,8,20,34], while the present study and some others considered discontinuity and irregularity of the root surface and loss of tooth structure as root resorption [24,31].
To the best of the authors' knowledge, the correlation of mandibular third molar impaction position and second molar root resorption and the effect of different positions   International Journal of Dentistry and angulations have not been adequately studied. Only three studies were found to report the most frequent impaction position and angulation of third molars [4,33,34], and two evaluated IMTM position [20,24]. e current results confirmed that occlusal surface position of IMTMs according to the Pell and Gregory classification, tooth position in relation to ramus according to the Pell and Gregory classification, and tooth angulation were associated with development of this pathological condition.
is could explain the different results of studies since one previous study reported root resorption caused by completely impacted mandibular third molars [24], while another study reported that partially impacted mandibular third molars were more capable of causing adjacent root resorption [20]. In this study, changing the angulation and greater depth of impaction relative to the reference level increased the risk of second molar root resorption, while changing the ramus relation with IMTM relative to the reference level decreased root resorption. A horizontal IMTM, class I ramus relation, and class C impaction level had the greatest association with distal root resorption of the adjacent second molar.

Relationship between Pathological Lesions and IMTM
Position. As bone density reduction was the most common pathological lesion investigated in this study, it was found that vertical, class Ш, and class C IMTMs had caused more pathological lesions. e most important factor responsible for development of pathological lesions was the IMTM position relative to the ramus such that any change from the reference level increased the risk of development of pathological lesions. However, with regard to depth of impaction and angulation, any change from the reference level decreased the risk of pathological lesions. Polat et al. reported that the prevalence of bone loss at the distal aspect of IMTM was 9.7% and it was found in association with distoangular and vertical IMTM positions [2].

Relationship between IAN Contact and IMTM Position.
e position and root location of IMTMs are among the most important factors associated with IAN damage [26,35]. In the present study, seven radiographic markers were used concurrently [19,25,[35][36][37][38][39][40]. ese markers were related to impaction depth and ramus relation according to the Pell and Gregory classification, and angulation of IMTMs [19].
e results of the present study revealed that 54.5% of IMTMs had contact with the mandibular canal, while 12.9% had contact with the external border of the canal. As contact with the mandibular canal can cause IAN neurosensory deficits after third molar surgery, a frequency of 54.5%-67.4% of contact with the canal can be considerable. us, in case of presence of signs of contact of IMTM with the mandibular canal, another imaging method such as conebeam computed tomography should be requested [41][42][43], although the sensitivity and specificity of cone-beam computed tomography were reported to be 93% and 73%, respectively, for this purpose [44].
Although class I and class II IMTMs showed higher frequency in terms of relation with the mandibular canal, class III had higher odds to be associated with the mandibular canal such that contact with the mandibular canal was observed in 75% of class III IMTMs (18 of 24 class III IMTMs), due to the anatomical position of the mandibular canal. Although class A IMTMs had higher frequency of contact with the mandibular canal, as expected, class B and C IMTMs had higher odds of contact with the mandibular canal. Mesioangular IMTMs showed greater contact with the mandibular canal, which was in agreement with other studies [19,45,46]. By an increase in impaction depth and changing the IMTM angulation from vertical to mesioangular and horizontal, risk of interference of the IMTM root with the mandibular canal increased. Also, class III cases had higher odds of interference with the mandibular canal than class I by 34%. By an increase in impaction depth, the odds of interference with the mandibular canal (contact with the canal wall and contact with the internal space) increased. IMTMs in horizontal position and class III IMTMs had significantly higher risk of interference of their root with the IAN, compared with contact with the external border of the canal; in other words, IMTMs in horizontal position and class III IMTMs had significantly higher risk of interference with the IAN and lower risk of contact with the external canal wall. In total, the frequency of complications associated with IMTMs was low but considerable in our study.  International Journal of Dentistry e occurrence of related complications with IMTMs is affected by the depth and angulation of impacted teeth. erefore, identifying IMTMs with higher risk of related complications can lead to early surgical intervention as soon as the first signs of pathologies arise; hence, regular followups are strongly recommended for such cases.
Long-term studies are suggested to evaluate the exact clinical and radiographic characteristics that favor retaining of asymptomatic IMTMs against their prophylactic extraction. Regular clinical and radiographic follow-ups are necessary until a comprehensive guideline is reached on this topic.

Conclusion
With regard to IMTM angulation, the frequency of all complications increased in mesioangular and horizontal positions except for pathological lesions. us, it may be concluded that mesioangular and horizontal positions are associated with higher risk of such complications. Distoangular position was also associated with higher risk of all complications, except for interference with the mandibular canal. In assessment of ramus relation, classes II and III were associated with higher risk of pathological lesions. Also, class III had higher risk of interference with the mandibular canal. In assessment of impaction depth, greater impaction depth was associated with higher risk of interference with the mandibular canal and root resorption.

Data Availability
e data used to support the findings of this study are available from the corresponding author upon request.

Conflicts of Interest
e authors declare that there are no conflicts of interest regarding the publication of this paper.