External apical root resorption after orthodontic treatment: analysis in different chronological periods

ABSTRACT Introduction: External apical root resorption (EARR) is characterized by the definitive loss of tooth root structure, with a higher incidence in lateral and central maxillary incisors. Objective: To identify, in different chronological periods, the incidence of EARR in the maxillary incisors (MI) of patients orthodontically treated with or without premolars extraction. Methods: Periapical radiographs before and after orthodontic treatment of 1,304 MIs from 326 patients (205 women and 121 men) were evaluated for EARR, divided into five groups, according to the chronological period in which treatments were started: G90) from 1990 to 1994, G95) from 1995 to 1999, G00) from 2000 to 2004, G05) from 2005 to 2009, G10) from 2010 to 2015. The evaluation was performed in each group, in patients who underwent maxillary first premolars extraction and those who did not. For statistical analysis, Fisher’s exact test was used, with a significance level of p < 0.05. The EARR was measured using the adapted Levander and Malmgren classification. Results: Incidence of EARR was higher in MIs of patients treated with maxillary premolar extraction (p < 0.05) in two chronological periods (G00 and G10), also being influenced by orthodontic treatments with longer duration, and due to possible individual genetic factors. Conclusion: Even with the limitations of a retrospective study, the lack of a defined EARR pattern in the MIs at different chronological periods was larger in the experimental group, due to the sum of factors such as premolars extraction, prolonged orthodontic treatment, possible genetic characteristics, and root shape, without the influence of the sex and age.


INTRODUCTION
Orthodontics has changed conduct throughout history. After Angle's death, one of his followers, Charles Tweed, evaluated previously treated cases without extractions and opted to retreat cases with relapses. Analyzing the cases treated without extractions, as recommended by Angle, he observed that 80% of the patients did not have adequate stability, facial aesthetics, periodontal health, and function. From that moment on, Tweed started to advocate extractions as an alternative to obtain facial harmony and greater post-treatment stability. 1 Due to these previously approached issues regarding stability, aesthetics and function after orthodontic treatments with extractions, tooth extractions for orthodontic reasons started to be more performed at the end of the 1940s. 2 Orthodontics finds itself in a conservative era, in which the tendency is to conduct treatments without extractions. Despite this non-extraction tendency, when correctly indicated, tooth extractions for orthodontic reasons are still considered the most appropriate therapeutic solution for some cases. 3 External apical root resorption (EARR) has been associated with orthodontic treatment, and is considered a collateral effect that culminates in the permanent and irreversible loss of tooth structure (dentin and/or cementum) 4

. Orthodontic forces with
Dental Press J Orthod. 2022;27(5):e2220100 Neves BM, Fernandes LQP, Capelli Junior J -External apical root resorption after orthodontic treatment: analysis in different chronological periods 5 different magnitudes have been associated to the incidence of EARR, as well as the severity it affects the teeth. 5,6 EARR can occur in any tooth during orthodontic treatment, being the maxillary lateral and central incisors the most frequently affected ones. 7 Levander and Malmgren 8 evaluated initial and final periapical radiographs of patients undergoing orthodontic treatment with a fixed appliance and classified the severity of EARR in five different levels, ranging from the absence of resorption to extreme resorption.
Regarding patients treated with conventional fixed appliances, more than a third of them usually have root resorption up to 3 mm. 9 Severe EARR is characterized by a loss of 5 mm of root length, and affects about 2% to 5% of orthodontic patients, imposing a risk to the function and maintenance of the resorbed tooth. 10 In orthodontic treatment, when the mechanical forces are interrupted, the EARR process also ceases; however, resorption can return and progress if tooth movement restarts, due to the application of forces. 11 Neves BM, Fernandes LQP, Capelli Junior J -External apical root resorption after orthodontic treatment: analysis in different chronological periods 6 A systematic review 12 showed that the application of forces at increased levels has a positive correlation with the increase in the amount of root resorption; as well as more prolonged treatments are related to greater resorption. In addition to these factors, a pause in tooth movement can be beneficial in these cases, because it allows the healing of the reabsorbed cement.
EARR is a consequence of an inflammatory process and presents some factors that may be related to its severity, such as: root shape, dental trauma, endodontic treatment, genetic predisposition, 13 age, 14 use of mechanical forces to perform orthodontic movements, and the duration of orthodontic treatment. 7 Thus, the present study aimed to evaluate the incidence of EARR on maxillary incisors (MI), in orthodontic treatments performed with or without extractions, in five different chronological periods, from 1990 to 2015, at the State University of Rio de Janeiro (UERJ, Brazil).

MATERIAL AND METHODS
In this unicenter retrospective study, in which a convenience sample was used, the documentation of 434 patients was evaluated,

MEASUREMENT OF EXTERNAL APICAL ROOT RESORPTION
Images of the periapical radiographs for the evaluation of EARR in the MIs were obtained using the method described by Fernandes et al 16     This measurement was performed in two stages: C1 (before orthodontic treatment, measured on the initial radiograph) and C2 (after orthodontic treatment, measured on the final radiograph).
2) Root size -measured from the central point of the CEJ line to the root apex, following the long axis of the tooth. This measurement was performed in two stages: R1 (before orthodontic treatment, measured on the initial radiograph) and R2 (after orthodontic treatment, measured on the final radiograph) (Fig 2). In cases of dilacerated root, the following measures were summed: from the central point of the CEJ line to the point of intersection between the long axis of the tooth and the dilacerated root portion, and from this point to the root apex, as shown in Figure 2.
3) Total tooth size: this measure was obtained with the sum of C1 + R1 and C2 + R2, resulting in the measures TT1 (total tooth size before orthodontic treatment) and TT2 (total tooth size after orthodontic treatment), as can be seen in Figure 3.   For the calculation and subsequent classification of EARR, the formula described by Linge and Linge 7 was used: R1-R2 [C1/C2], in which the amplification factor is defined by C1/C2, assuming that the crown size did not change during the treatment.

CLASSIFICATION OF INCISORS ACCORDING TO EARR
Each of the 1,304 MIs was measured for EARR using the Image The software Statistical Package for Social Sciences v. 23.0 (SPSS Inc., Chicago, IL, USA) was used for data analysis.
As this was non-parametric data, it was not necessary to verify the normality of the sample, 17 and the data were then characterized as non-normal distribution with more than two groups, with independent samples. Considering the needs of the described sample, Fisher's exact test was selected to assess whether there was a difference in the EARR in the MIs in the different chronological periods in patients who had undergone maxillary first premolars extraction, considering the power at 95% with a significance level of 5%.

RESULTS
In the descriptive analysis of the data, 1,304 incisors were evalu-   Taking into account that rhomboid roots were less affected by EARR than pipette-shaped and dilacerated roots, which were more affected by EARR, 18,19 when analyzing the distribution of root shape in the different chronological periods, in the G00, the percentage of rhomboid roots was considerably higher in the CG than in the EG; making the CG teeth less susceptible to EARR (Table 1).
To analyze the data obtained in the statistical analysis related to the incidence, the EARR was evaluated on the four incisors of Neves BM, Fernandes LQP, Capelli Junior J -External apical root resorption after orthodontic treatment: analysis in different chronological periods Two examiners were calibrated to assess the measurements: E1 (examiner 1) and E2 (examiner 2), for evaluating the intra-examiner and inter-examiner Regarding the duration of treatment, the different chronological periods showed variations that should be considered in the evaluation of results: in these periods, treatments with extractions had a longer duration in EG, whereas in G00 the difference in treatment time was 3.15 years and in G05 was 0.9 years (Fig 4).
The treatments had a longer duration mainly in patients treated with extractions of premolars; however, the treatments performed without extractions in the different chronological periods also had a duration considerably longer than desired. It can be seen that from 1990 to 2000, the treatments with extractions showed a duration increase, and from 2005 onwards, there was a reduction in this time, reducing even more from the year 2010 (Fig 4). This variation can be credited to the duration of treatments in parts, to the differences in the conduction of the treatments, as well as the collaboration of each patient. It is important to highlight that the G10 group presented a smaller number of treated patients, due to the proximity to the time when this study was realized..
Taking into account the sex variable, the sample was heterogeneous, with different distributions according to chronological periods, as showed in Table 3.

DISCUSSION
During the development of this study, some factors that could influence EARR were evaluated, to try to explain the statistically significant higher incidence of EARR in patients in G00 and G10: in G00, teeth #12, #11, #21, and #22 were more affected by EARR in patients treated with maxillary first premolars extraction, as well as tooth #21 from patients in the G10.
This could be because EARR has a multifactorial etiology that comes from a complex interaction between the effect caused by mechanical forces applied during active orthodontic treatment and the patient's biology. 21 CG = control group. EG = experimental group.
Neves BM, Fernandes LQP, Capelli Junior J -External apical root resorption after orthodontic treatment: analysis in different chronological periods 20 The individual or biological characteristics of the patients mentioned in this study are more specifically related to the genetic component of each patient, as well as their genomic information, which will determine or will codify proteins and signaling mechanisms related to root resorption or repair of cementum and dentin during orthodontic treatment. 22  the fact that, as treatments performed in the CG demanded a shorter duration, these teeth would be less susceptible to EARR.
Some authors 36,37 demonstrated that there is a relationship between EARR and dental extractions in patients who have undergone orthodontic treatment. In the study by Fernandes et al, 16 the authors concluded that the risk of developing EARR greater than 2 mm in MIs is 70% higher in patients treated with premolars extraction. In another study 38 in which EARR was also evaluated in patients with and without extractions, patients treated with extractions of first premolars showed greater resorption in the MIs than those treated without extractions.
In the present study, there was a significant difference in the occurrence of EARR in two chronological periods of orthodontic treatment beginning (G00 and G10), with greater EARR in some groups of teeth in EG patients, when compared to CG patients, corroborating the results from previously cited studies, which show that treatments with extractions influence EARR, when compared to treatments without extractions. 16,[36][37][38] Regarding the orthodontic mechanics used to perform the treatment of patients allocated to the EG, this factor could not be correlated to the EARR, considering that the EARR occurred without a defined pattern. Except for two cases, the retraction of the maxillary incisors and canines was performed in two phases, being the first phase for canines distalization with an elastomeric chain; and in the second phase, after the canines were