An Insight into Risk Factors for Root Resorption During Orthodontic Treatment

INTRODUCTION

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The term ‘Orthodontically induced inflammatory root resorption’ (OIIRR) is mainly used in orthodontic to differentiate from any other causes of root resorption in permanent teeth¹. It is inevitable as the force applied during orthodontic treatment induces inflammation which is essential for tooth movement, however it is also a fundamental component for root resorption.

In order to minimize the degree of root resorption, optimum force level is suggested to be within 20-150 g tooth‾¹ for desired tooth movement². Force level exceeding this threshold can cause periodontal ischaemia especially in adults as they induce more apical stress due to thicker cementum when compared to adolescents³. Apical region is more susceptible to root resorption than the cervical region, since it is softer and less mineralized and contains fewer sharpey’s fibers. Furthermore, the region where periodontal ligaments are compressed during tooth movement increases the risk for root resorption.

Root resorption is a common side effect during orthodontic treatment, however it usually ceases and repaired when the force is removed. Although, OIIRR is unavoidable in orthodontics, it usually occurs at mild degree with radiographic mean resorption⁴ of less than 2.5 mm. Although, the event where root resorption becomes progressive is minimal, it will reduce the prognosis of the tooth and in severe cases, may become mobile and consequently jeopardized the initial treatment plan. Therefore, it is important for orthodontists to identify risk factors for root resorption even before starting orthodontic treatment^5,6. Modification on treatment mechanics may be suggested to minimize the occurrence of root resorption during orthodontic treatment.

The OIIRR is a complex and sterile inflammatory process of which many aspects still remain unclear. It has been a debate for many years on certain patient characteristics and treatment modalities as risk factors for OIIRR. Justus⁴highlighted genetic predisposition as the main aetiologic risk factor for severe form of OIIRR⁴. This study provides the most current view, over the past 6 years (2010-2015), on the multiple risk factors of root resorption so that the clinical management for minimizing root resorption during orthodontic treatment can be addressed appropriately.

All reported studies were identified electronically through PubMed, Scopus and ScienceDirect with the key words of ‘risk’,‘root’,‘resorption’ and ‘orthodontic’ covers until year 2015. The findings of the risk factors were divided further into host and treatment mechanic factors.

PREVALENCE OF ROOT RESORPTION DURING ORTHODONTIC TREATMENT

Prevalence of root resorption during orthodontic treatment reported^5,7 variation from 4-91%. It is found that almost all patients and up to 91% of all teeth showed some degree of root shortening but few patients and teeth had root shortening⁷ of >4 mm. Pereira et al.⁸ reported percentage in external apical root resorption varies on each anterior teeth ranging from 8.5% for upper right canines, to 12.6% for upper right lateral incisors, with significant higher root resorption in incisors than canines. Makedonas et al.⁵ reported 4% of patients were diagnosed with root resorption after 6 months of fixed appliances with only 3.1% of maxillary incisors involved. Marques et al.⁹ found 14.5% prevalence of severe root resorption while Motokawa et al.¹⁰ found high incidence of 78.2% in their study. Matsuda et al.¹¹ also reported 78% patients with root resorption at the end of orthodontic treatment.

Reports of these prevalence of root resorption have to be closely monitored as they can be mistakenly interpreted. Some studies reported their prevalence in relation to number of patients and others in the number of teeth^5,7,11. It does differs as proven by Motokawa et al.¹⁰, where the researchers separated the results for evaluation of prevalence of root resorption by number of teeth and patients. It is found that for severe root resorption, no significant differences were found in the number of patients but when evaluated by the number of teeth, the prevalence was significantly greater in the extraction than in the non-extraction group.

Other factor that can be contributed to the variation of prevalence of root resorption during orthodontic treatment is the assessment methods. There are two techniques in discovering the presence of root resorption which are by histological or radiographically. Histological finding was performed either on animal teeth or human premolar extracted teeth due to the necessity to observe the teeth in vitro^12-21. The advantage of investigating root resorption histologically is that it can be observed directly on the root surface and even the smallest craters can be noted. The measurement of root resorption was usually presented in the reduction of root length (millimeters) or increased in volume of resorption craters (cube root scale-millimeters).

Evaluating root resorption through radiograph is more related to clinical practise and many researchers had favored 3D images such as cone beam CT and micro-CT in detecting root resorption during orthodontic treatment as compared to 2D images such as periapical, panoramic and lateral cephalometric^{5-8,10,18,21-30}. Higher prevalence of root resorption is expected in 3D images as the view eliminates overlapping structure and allow for better visualization of specific tissue volume⁷. However, the disadvantages of 3D imaging are more on the technical aspect; where it has higher radiation compared to 2D images and access for view is only through its software. Nevertheless, the advent of CBCT has reduced its radiation, making it an advantageous tool in dentistry.

MONITORING OF ROOT RESORPTION AND POTENTIAL BIOMARKERS DURING ORTHODONTIC TREATMENT

It is difficult to detect root resorption early as the event is usually noted only when radiograph is taken. However, radiographs have the limitation of radiation exposure, the way it is handled, standardization and limited points of view. Several protocols suggest that radiographic examination should take place in the first 3-6 months and then every year after appliance placement. The practical usage of the first radiographic evaluation in the first 6 months to diagnose and predict OIIRR has not yet been studied thoroughly⁵.

Given these limitations, hence the current trends of finding biological markers for root resorption which essentially provides sensitive, safer and more prognostic diagnostic methods for detecting root resorption³¹. Protein markers such as aspartate aminotransferase, salivary sIgA and serum IgG as well as biomarkers representing biological changes during specific phenomenon during orthodontic tooth movement such as ALP (bone formation), TRAP5a (bone resorption), LDH (inflammation) and DSP (root resorption) was found to have potential for detecting root resorption^32,33.

George and Evans³⁴ tested the hypothesis that during root resorption, organic matrix proteins and cytokines from the surrounding bone and dentin are released into the gingival crevice and the preliminary results confirm of their presence. The OPG was locally present in excess amounts over RANKL and an increased RANKL/OPG in the study groups could be correlated with an increased bone resorption activity during orthodontic tooth movement.

Mah and Prasad³¹ and Kereshanan et al.³⁵ found high level of DSP (dentine siolaprotein) and DPP (dentine phosphoproteins) respectively on sites undergoing physiological root resorption. These proteins are parts of 10% of the organic matrix in dentine composition as non-collagenous proteins³⁶. Although, DSP is found in some control sample, it was in reduced level, suggesting that it is dentine specific. Therefore, there is a strong indication that the presence of DSP or DPP is an indication of undergoing root resorption³⁵.

Fig. 1:	Score system categorizing the severity of root resorption by Levander and Malmgren37 based on index score from 0-4

Fig. 2(a-e):	Subjective scoring of root form by Malmgren et al.39. The shape of the roots was classified as, (a) Normal, (b) Short, (c) Blunt, (d) Bent at the apex and (e) Pipette form

CLASSIFICATION OF ROOT RESORPTION SEVERITY

The categorization of root resorption severity also differs in studies which would vary the prevalence of root resorption. Levander and Malmgren³⁷ root resorption scoring system (Fig. 1) with index scores from 0-4 is the most commonly used to classify the severity of root resorption^{5,6,9,27,29,38}. However, some studies reported their findings in reduction of the root length without categorizing the severity of root loss^{12,13,15,16,18,19,21}. In the study of abnormal root shape as the risk factor for root resorption, most studies follow guidelines which was introduced by Malmgren et al.³⁹ (Fig. 2), where the roots were differentiated between short, blunt, apical bent and pipette shaped.

Treatments received by the subjects in the study also had contributed to wide range of prevalence of root resorption and this will be further discussed in the later part of this review. Types of appliances, the forces used and duration of treatment which were set as the control in the studies may somehow increase or decrease the percentage of prevalence as they are proven to commit as risk factors for root resorption.

RISK FACTORS FOR ROOT RESORPTION

Risks factors are divided into host and treatment mechanics. Host factor means that it is patients-originated; for example gender, race, history or the condition and location of the teeth and it is beyond control of the clinician. Clinician can only screen for high-risk patients and the risks of root resorption from host factor need to be fully considered when planning for an orthodontic treatment. Treatments mechanics factors are more of a concern by the clinician as these can be manipulated and amenable via modifications during orthodontic treatment to reduce progressive root resorption.

Host factors: Gender differences in the risk of root resorption were investigated and male was found to have a higher chance of root resorption as compared to women^8,11. Nevertheless, there were studies that proved that there was insignificant difference in gender in relation to root resorption^{7,10,13,18,21,38}. As far as age concern, patients above 20 years old may have significant relation to root resorption but most of the studies found age is not a risk factor for root resorption^{8,11,18,21,38}.

Teeth with root resorption even before orthodontic treatment, whether of physiological or pathological reasons, have proven to be associated with progressive root resorption during orthodontic treatment⁹. Physiological root resorption can occur as a consequence of an adjacent impacted tooth. The most common problem with impacted canines is resorption of the roots of the adjacent lateral incisors or premolars. Oberoi and Knueppel²⁸, on the study of 3D assessment of impacted canines and root resorption reported 40.4% of lateral incisors have no resorption, 35.7% with slight root resorption, 14.2% moderate root resorption and 4.0% with severe root resorption. Another study on Chinese population reported that eruptive movement or migration of the impacted canines during its root development process is likely to increase the risk of root resorption. The eruptive movement of canines during root development might cause mechanical and molecular changes to the local environment involving adjacent roots. This was proven with significant increase in root resorption of adjacent root on closed apex canine when compared to open apex canines. Physical proximity of less than 1 mm between impacted canine and adjacent roots is also the most important predictor for root resorption at the incisors and first premolars³⁰. Root resorption which occurs at the adjacent roots may be caused by direct physical damage, increased pressure at local root cementum and dentin or concentrated resorptive molecules from the canine eruption follicle.

Brusveen et al.²³ had demonstrated in order to disrupt the resorptive process, the impacted canine has to be distanced from the adjacent roots. In the study, canine retraction during orthodontic treatment was done by pulling it away from the adjacent incisor roots via a specially constructed transpalatal arch with a finger spring. Fixed appliances on the incisors were only applied as late as possible, after canine eruption. The protocol was done as such, that they could not support the hypothesis that an impacted canine is a risk factor for apical root resorption of incisors. Even after 13-28 years post-treatment, most cases of incisor root resorption induced by ectopic maxillary canine did not progress and showed no clinically relevant symptoms²².

Anterior open bite was also a significant factor for Orthodontically Induced Inflammatory Root Resorption (OIIRR) with the speculation of the jiggling force caused by orthodontic force and tongue pressure to move the teeth in opposite direction^8,38. Most cases with an anterior open bite may end up with extraction of premolars as the treatment plan but Pereira et al.⁸ found that these two factors, anterior open bite and extractions of premolars were independent of each other. In the study, patients with open bite only had 26.1% of OIIRR, approximately similar to open bite patients submitted to premolar extractions which had 26.0% of OIIRR.

Abnormal root shapes had always been associated with root resorption and it is in agreement with recent studies^27,38,40. Root forms are usually classified as normal, short, blunt, bent at the apex and pipette form (Fig. 2). It was speculated that abnormal root shape causes root resorption due to reduced resistance of the root to mechanical stimuli. The prevalence of root resorption is greater in abnormal root shape with hypofunctional teeth than in functional teeth. It was suggested that the reason might be that non-occlusion in hypofunctional teeth did not cause physiological root remodeling after teeth eruption hence development of root resorption³⁸. A case study on rare condition of short root anomaly on maxillary and mandibular incisors noted of a girl aged 10 years old that had a treatment of functional appliance²⁷. There was significant mobility in the mandibular incisors at the termination of wearing functional appliances which was then decided to be retained with fixed lingual retainer. Although it is reported that no change in the amount of root shortening, caution must be taken in deciding which treatment is the best for each patient.

Other host factors in the risk of root resorption such as root canal treatment and history of trauma were also reported. Kaku et al.¹⁷ showed that teeth with root canal treatment may be a predictor for progressive severe inflammatory root resorption during orthodontic tooth movement while Makedonas et al.⁵ found no statistically significant relationship of root resorption with the risk of trauma. Makedonas et al.⁵ also found no statistically significant on relationship of root resorption with the risk factors of finger sucking, finger sucking history, nail biting and nail biting history after 6 months of wearing fixed appliances. The significant and insignificant finding for host risk factors in root resorption during orthodontic treatment is presented in Table 1.

Treatment mechanics factors: Some of the orthodontic treatment mechanics that are applied in the clinic are inevitably related for increasing the risk of root resorption.

Table 1:	Significant and insignificant studies of host risk factors for root resorption during orthodontic treatment

Longer duration of orthodontic treatment had been proven to be one of them^6,10,19,29. Motokawa et al.¹⁰ studied on the effect of duration of multiloop edgewise archwire (MEAW) treatment, elastics and total treatment time on root resorption. For the duration of MEAW, there is significantly higher prevalence of severe root resorption, evaluated by number of teeth and in long term use of elastics (>6 months). Total treatment time of more than 30 months was proven to have increased the risk of severe root resorption when evaluated both by number of patients and teeth. Long duration of orthodontic treatment exposes the teeth to long term jiggling force causes an increase in root resorption.

The duration of force applied at one time, whether continuous or intermittent forces was also in the investigation for the effect in root resorption. Aras et al.¹² found that although the continuous force produces faster tooth movement than intermittent forces, it brings higher risk in root resorption. Intermittent force allows time for reparative mechanism thus produces less root resorption. Paetyangkul et al.¹⁹ studied the root resorption craters histologically with 4 or 8 weeks of retention after application of continuous light or heavy orthodontic force. New cementum layer had almost repaired resorption cavity of root in 8 weeks retention group, unlike the 4 weeks retention group, resorption craters were still repairing with new cementum and presence of inflammatory infiltrates. From these studies it can be concluded that the reparative cementum is time-dependent and tooth movement is efficient when the force is given intermittently, for longer period of time. The method of applying intermittent force was mentioned by Justus⁴ in his book as one of the treatment options if root resorption is pronounced in the radiograph during the middle of orthodontic treatment. Activation of archwire once every 2-3 months are preferable instead of monthly.

Depending on the force direction and root morphology of the tooth, the compression area on root surface is more susceptible to root resorption than in tension area²¹. Study on tipping tooth movement and buccal root torque of 2.5 and 15° on extracted premolars also agreed with increase of root resorption on root area of compression^13,18. During tipping movement, periodontal ligament compression was more pronounced in the apical and cervical thirds of the tooth whereas in buccal root torque, the root resorption was seen more on the apical. Intrusion was indicated as the most deleterious tooth movement as the force is directed and compressed on the small apical region of the tooth. A comparison between two groups which had en masse retraction of upper incisors with and without intrusion with minis crews showed a significant apical root resorption of lateral incisors, not in central incisors, in retraction group with minis crews²⁶. Mechanics of intrusion with micro implant when comparing to J-hook during retraction of upper anterior segment also proved significant root resorption⁴¹.

New approach for reducing the amount of root resorption during intrusion was proposed by introducing lighter and more continuous force as well as control of force vector and labiolingual position of the tooth²⁴. This was proven in several studies that heavy force applied beyond its optimum for tooth movement will increase the risk of root resorption^{15,16,18,19,21}. One study proved contradictly, where histological evaluation of mandibular teeth in beagle dogs found that constant intrusive forces between 50-200 g produced similar degree of root resorption, regardless of the force magnitude²⁰.

During functional appliances, teeth that are used for anchorage will sustain great amount of force as patient is expected to wear the appliance full time. This, theoretically, will favor the development of root resorption. However, in teeth with incomplete root formation, this was proved otherwise, Kinzinger et al.²⁵ focused on growing patients of class II malocclusion wearing Herbst appliance.

Table 2:	Significant and insignificant findings of risk factors for root resorption during orthodontic treatment (Treatment mechanics factors)

From this study there was a tendency towards root length decrease in teeth with complete root formation but significant increase in root length of teeth with incomplete root formation at the start of the treatment. Teeth with incomplete root formation has wide open apical foramen which ensure the pulp still retain its vitality as fewer blood vessels are compressed, otherwise might be involved in resorptive developments even at the strong forces. Therefore, it is suggested that if Herbst appliance or any types of functional appliance are indicated in the treatment plan, the treatment should starts early when the root is still developing as they have higher biologic tolerance. This statement was also supported by Maues et al.⁶, in which they find teeth with complete root formation were more likely to develop severe root resorption compared to teeth with incomplete root formation at the onset of treatment.

Nevertheless, optimum force during intrusive movement is important to balance the benefit of intrusion movement and disadvantage of root resorption. It was assumed that the optimum force for intrusion is similar whether the technique is conventional or using minis crews²⁴. Extrusion movement also cause root resorption but the results showed insignificant difference in the cervical, middle and apical thirds in relation to root resorption after light and heavy force¹⁶.

Teeth extraction is usually a treatment option for relieving crowding and reduces overset in malocclusion however it does come with consequences. Premolar extraction was found to have significant risk for root resorption and this could be related to distance that canines and incisors are moved^{6,8,10,27,29,40}. The anterior segment is retracted several millimeters after premolar extraction, especially in the case of high incisor protrusion. Motokawa et al.¹⁰ found significant difference in the prevalence of severe root resorption evaluated by number of teeth in extraction than in non-extraction group. Extraction of premolars increases the amount of tooth movement and also requires longer duration of treatment to close the extraction space. Motokawa et al.¹⁰ also found that displacements of maxillary central incisors and changes in tooth inclination were significantly larger in the group with severe root resorption than in the group without resorption. Therefore it can be concluded that apical vertical movements and incisor proclination are strong predictors of external apical root resorption.

Motokawa et al.¹⁰ also found no significant difference in the prevalence of root resorption between two groups with and without surgery. This is subjected to evaluation of both by the number of patients and teeth. This study was performed based on the believe of increase in chronic tongue pressure and circumoral muscle tonus after surgical treatment might rise the prevalence of root resorption. All these latest findings of treatment mechanics risk factors during root resorption in orthodontic treatment patients are presented at Table 2.