The correlation between external apical root resorption and electric pulp test responses: a prospective clinical trial

ABSTRACT Objective: The current study investigated the correlation between pulpal sensitivity to the electric pulp tester (EPT) and external apical root resorption (EARR) in four types of maxillary anterior teeth of fixed orthodontic treatment patients. Methods: In this prospective cohort study, 232 anterior teeth of 58 patients (mean age 18.96 ± 6.13 years) treated with fixed orthodontic treatment were examined. The EPT readings were recorded at twelve time points immediately before archwire insertion. Root resorption of four maxillary incisors were measured by means of parallel periapical radiographs at three time intervals (six months interval from the start) through design-to-purpose software to optimize data collection. A multiple linear regression model and Pearson correlation coefficient were used to assess the association of EPT values and observed EARR (p< 0.05). Results: The highest level of EPT measurement was recorded at initial visit, and then there was a decreasing trend in EPT level during treatment for the next six and twelve months. There was another increasing trend after six months till the finishing time of the treatment. There was a significant correlation between changes in root length and time of recording the root length (p< 0.001). There was significant positive correlation between changes in EPT level and amount of observed root resorption (p< 0.001). Conclusion: The relative decrease in electric pulp test level could be a diagnostic sign of root resorption during orthodontic treatment. Further studies with longer follow up are needed to confirm the current results.


INTRODUCTION
External apical root resorption (EARR) occurring in permanent teeth during comprehensive orthodontic therapy is a common iatrogenic phenomenon. 1 Histologically, orthodontically induced external apical root resorption has been reported to occur with an incidence greater than 90%. However, the radiographic incidence is lower, at approximately 48-66%. 2 The underlying causes of this unwanted process can be divided into two broad categories, biological and mechanical aspects. 2 Mechanical factors include orthodontic treatment-related risk factors, such as treatment duration, magnitude of applied force, direction of tooth movement, amount of apical displacement, and method of force application. 3 The maxillary incisors are the teeth most affected by root resorption, followed by the mandibular incisors and first molars. EARR occurs in different degrees of severity. Severe EARR is defined as a shortening greater than 4 mm or one-third of the root length, and is observed in 1-5% of teeth. 3 3D imaging (CBCT) has shown to be radiographically valid and reliable in the assessment and diagnosis of EARR. However, considering the potential radiation risks of 3D imaging, the most common diagnostic strategies for root resorption remains 2D conventional images, as panoramic and periapical radiographs, and lateral cephalometries. 4 Panoramic and lateral cephalometries have been proposed to be more applicable for Younessian F, Behnaz M, Badiee M, Dalaie K, Sarikhani A, Shekarian S, Kavousinejad S, Ebadifar A The correlation between external apical root resorption and electric pulp test responses: a prospective clinical trial 5 measurement of EARR, considering their significant advantages of less radiation exposure, visualization of the complete dentition, less time-consuming for the operator, and more patientfriendly, compared to very recent micro-CT three-dimensional methods. 5 However, they are still considered to be less accurate than periapical films, and overestimate the EARR by 20% the amount of root loss. 6,7 Furthermore, periapical films are prone to magnification errors. According to the recent study by Pereira et al, 8 this magnification error may be overcome by using the percentage of root/tooth variation, instead of direct measurement of root resorption. Recent advances in the digital image processing and artificial intelligence techniques have made it possible for the computer-assisted superimpositions to be done more accurately, and have increased their clinical applicability. If any root resorption is diagnosed, an inactive phase of 4 to 6 months before the resumption of orthodontic treatment is currently advocated. 5 Unfortunately, early detection of this condition could not be accomplished before six months from the beginning of resorption. 9 To date, many studies have evaluated the effect of orthodontic forces on the dentin-pulp complex. 10

SAMPLES AND SAMPLE SIZE CALCULATION
In this prospective non-controlled cohort study, 58 patients (42% male; age range 12-35 years; mean age 18.96 ± 6.13 years) who were referred to the orthodontic department of School of Dentistry, Shahid Beheshti University of Medical Sciences, were selected using random-cluster sampling method. Sample size was determined to be equal to 50 patients (200 anterior teeth sample size) considering α = 0.05, β = 0.20 (power equal to 0.80) and r = 0.2 (low effect size), using sample size calculation software v. 3.0.43. Considering the possibility of dropouts to be 20% during the study, we enrolled 58 patients with 232 anterior teeth. The exclusion criteria were the presence of congenital, systemic or concomitantly diagnosed serious medical conditions, allergy, asthma, familial dysostosis and also history of dental trauma before or during the study, history of lingered pain to thermal stimuli, open apex, any medication, history of previous root resorption, extraction treatment regimen (crowding greater than 7mm in any arch) and also presence of parafunctional habit. Those whose radiographs lacked visibility of maxillary incisors, those with significantly distorted radiographs, crowding of teeth (greater than 7mm in any arch), unclear roots and those with unilaterally and bilaterally lateral missing teeth in the maxilla were also excluded. Those patients who missed to attend their regular monthly follow up or diagnosed with other treatment plans like removable appliances or orthognathic surgery were also excluded from the study. Healthy periodontium (probing depths not exceeding 3 mm, no bone loss as determined by radiographs) and dentition (no carious lesions, no endodontically treated maxillary incisors and closed apex) were necessary to enroll in this study.

Examination of periapical radiographs
The original periapical radiographs of all three groups were obtained with the same digital X-ray unit (KODAK 2100 Intraoral X-Ray, at the same distance and using the same exposure settings: 60 kvp, at 7 mA, 0.2 s). All radiographs were exported and saved in JPEG format using the Digora ® software, v. 2.8.
The digital radiographs were then visualized and analyzed using Photoshop CS (Adobe Systems Inc., San Jose, CA, USA).
A magnification of up to 150% was applied when necessary.
All the periapical radiographs were taken in natural head positions, and the examiners used the scanned version of the radiographs.  To standardize the parallel periapical radiographs, a correction factor was calculated based on the assumption that the crown length had to remain unchanged. Therefore, the ratio C 1 /C 2 (pre- could determine the inconsistency between crown lengths of the two X-rays, and was used to compensate for the enlargement factor. Apical root resorption was then calculated as follows: Root resorption = 1-(CR 2 /R 1 ), Where CF is the correction factor, C 1 and R 1 are the crown length and root length in pretreatment X-rays, while R 2 and CR 2 are root length and corrected root length in post-treatment X-rays, respectively. The point marking process was done on an enlarged version of the X-ray, to help reduce the error.
Furthermore, the operator repeated the markings five times on each pair of X-rays, recorded the software output after each marking, and used the averaged value as the final root resorption.

Electric Pulp Test (EPT)
Electrical stimulation was provided by the digital electrical pulp To prevent any temperature change and false responses, patients were asked to not eat or drink ten minutes before each visit. After removal of orthodontic archwires, every tooth was isolated with cotton rolls and dried thoroughly before EPT evaluation. The testing site was confined to sound enamel on the midpoint incisal edge of each tooth. This is necessary in order to avoid the orthodontic brackets, and to minimize the

Root length alterations
The radiographs of 58 patients (42% male; age range 12 to 35 years; mean age 18.96 ± 6.13 years) participants were evaluated. Two of the samples were excluded and replaced because of unclear periapical radiographs. Mean and standard deviation of the root length measurement is demonstrated in Table 1.

EPT levels
EPT changes from T 0 to T 12 are demonstrated in Table 2 and Comparing the twelfth month with baseline, EPT level was also significantly reduced (p < 0.001). However, the reduction in the second six months was not significant comparing to the first six months (Fig 3).

Correlation of age with root resorption, and age with EPT response
Age did not demonstrate significant correlation with the amount of observed root resorption (p = 0.497). Therefore, the selected age range in this study (mean age 18.96 ± 6.13 years) has no statistically significant effect on root length alterations in time.    (Table 3).

DISCUSSION
External apical root resorption (EARR) is a common adverse outcome of orthodontic tooth movement. This unwanted phenomenon is seen mostly in teeth that underwent heavy orthodontic forces for long period of time. EARR is also seen in teeth with weak periodontal support. 14 Various factors including biological and mechanical elements are responsible for the initiation of EARR and its progress during orthodontic tooth movement. 15,16 The most common teeth to undergo EARR are the maxillary incisors and maxillary and mandibular canines, with the average amount of 0.2 to 2.93 mm.
The possible controversy regarding the average amount of EARR between studies is mostly due to difference in sample The error level of periapical radiographs is four times less than cephalometry radiographs. 17 Evaluation of the root length in three different time intervals demonstrated that there was a significant reduction in the root length at both time points, compared to baseline (p < 0.001). The root length also was significantly reduced between the sixth and twelfth months of study (p < 0.001).
As orthodontic tooth movement creates inflammatory responses in bone and periodontium, the release of some inflammatory cytokines, including prostaglandins and leukoterins, will occur and increase the possibility of root resorption. 18 These cytokines increase the vascularity of the regions under orthodontic force. Therefore, pre-osteoclasts The effect of orthodontic force on dental pulp is evaluated in various studies in the literature. 23 There is no general consensus regarding the effect of orthodontic forces on dental pulp, and these contradictory results could be due to differences in sample size and type of tested tooth. 13,24 Additionally, evaluation of dental pulp necrosis requires a histopathologic evaluation that is not clinically possible for most cases. Another method is using an electric pulp test (EPT), which is a non-invasive, easy and cost-effective method to evaluate nerve response to orthodontic tooth movement. 24 26 study is that without any evidence-based risk factor of root resorption, clinicians could use EPT records as diagnostic tool, to prevent severe root resorption before being evident in panoramic radiographs.
Further studies with larger sample size and follow up until conclusion of orthodontic treatment are needed to confirm the current results. As EPT only provides information on the status of pulpal nerves, and does not directly determine the vitality (vascularity) of pulp, it is also suggested to repeat the study with vascular measurement techniques, instead of nerve response measurement, which could be a more valid measure to be attributed to root resorption sequel in teeth undergoing orthodontic tooth movement. 28  2. The highest level of EPT response was at the first visit and then reduced over time, with slight increase in last months.
3. There was no significant association between type of tooth and observed root resorption, however the association between EPT level change and root resorption was significant.

The association between root resorption and EPT levels
demonstrated that for each unit reduction in EPT level, a 0.02-mm root resorption was observed. Overall responsibility:

MBe.
The authors report no commercial, proprietary or financial interest in the products or companies described in this article.