Root Resorption in Orthodontics: An Evidence-Based Approach

Root resorption is a pathological process that causes a shortening of the dental root. Although this condition is generally asymptomatic and missed in diagnosis, it may result in tooth mobility and even tooth loss if not diagnosed and treated early (Ahangari et al., 2010). In orthodontics, induced inflammatory root resorption is a form of pathologic root resorption related to the removal of hyalinized areas of the periodontal ligament following the application of orthodontic forces and is considered an undesirable but unavoidable iatrogenic consequence of orthodontic treatment (Brezniak & Wasserstein, 2002a; Brezniak & Wasserstein, 2002b).


Introduction
Root resorption is a pathological process that causes a shortening of the dental root. Although this condition is generally asymptomatic and missed in diagnosis, it may result in tooth mobility and even tooth loss if not diagnosed and treated early (Ahangari et al., 2010). In orthodontics, induced inflammatory root resorption is a form of pathologic root resorption related to the removal of hyalinized areas of the periodontal ligament following the application of orthodontic forces and is considered an undesirable but unavoidable iatrogenic consequence of orthodontic treatment (Brezniak & Wasserstein, 2002a;Brezniak & Wasserstein, 2002b).
The root resorption may compromise the continued existence and functional capacity of the affected tooth, depending on their magnitude (Brezniak & Wasserstein, 1993a, Brezniak & Wasserstein, 1993b, since the root structure (volume and contour) is changed (Consolaro, 2002). However, as the process of root resorption during orthodontic treatment is usually smooth and ends when the force is removed Levander et al., 1994) some authors have pointed out that the aesthetic and functional improvements justify the risks .

Aims of the chapter
The aims of this chapter are to give a detailed description of root resorption, how it begins, the mechanisms involved in this condition and how the risk factors described in the literature contribute toward the development of root resorption related to orthodontic treatment. The importance of a thorough patient history and early diagnosis are also discussed. The value of high-quality research, such as longitudinal cohort and prospective studies, randomized clinical trials, systematic reviews and meta-analysis, is stressed in light of the current emphasis on evidence-based dentistry. Care and recommendations, legal implications and a case description of a patient with root resorption following orthodontic treatment are also presented.

How root resorption begins?
Orthodontic tooth movement is based on force-induced periodontal ligament and alveolar bone remodeling (Abuabara, 2007). So, orthodontic forces represent a physical agent capable of inducing inflammatory reaction in the periodontium (Giannopoulou et al., 2008). When a tooth moves, a necrosis of periodontal ligament on the pressure side with formation of a cell-free hyaline zone occurs. This event is followed by osteoclast resorption of the neighbouring alveolar bone and bone apposition by osteoblasts on the tension side (Abuabara, 2007). The resorption process of dental hard tissues seems to be triggered by the activity of some cytokines as well as that of bone. Immune cells migrate out of the capillaries in the periodontal ligament and interact with locally residing cells by elaborating a large array of signal molecules (Jäger et al., 2005). According Consolaro et al. (2011), the causes of root resorption should be related to the loss of root surface cementoblasts.

Orthodontic treatment-related factors
The ideal force for tooth movement would mimic a physiologic balance between tooth movement and bony adaptation (Paetyangkul et al., 2009). Schwarz (1932) advocated the optimal force level for tooth movement between 7 and 26 g per square centimeter. He also stated that, when force exceeded this threshold, root resorption occurs. When pressure decreases below this limit, root resorption ceases . This was later confirmed by King and Fischlschweiger (1982), who found that light forces produced insignificant root resorption, whereas intermediate or heavy forces resulted in substantial crater formation.

Treatment duration, force application method and magnitude of the applied forces
In a study, Acar et al. (1999) compared a 100-g force with elastics in either an interrupted (12 hours per day) or a continuous (24 hours per day) application. Group who has teeth experiencing orthodontic movement had significantly more root resorption than the control group. Besides that, continuous force produced significantly more root resorption than discontinuous force application.
Later, Ballard et al. (2009) conducted a prospective randomized clinical trial to compare root resorption with two force application patterns (continuous and intermittent) and they concluded that the application of intermittent orthodontic forces of 225 cN for 8 weeks (14 days of force application, 3 days of rest, then 4 days of force application repeated for 6 weeks) caused less root resorption than continuous forces of 225 cN for 8 weeks. The authors stated that, although it might not be clinically practical, compared with continuous forces, intermittent forces might be a safer method to prevent significant root resorption.
More recently, Paetyangkul et al. (2011) investigated the amounts of root resorption volumetrically after the application of controlled light and heavy forces in the buccal direction for 4, 8, and 12 weeks. They found significant differences in the extent of root resorption between 4, 8, and 12 weeks of force application (P < 0.001), with substantially more severe resorption in the longer force duration groups. The light force produced significantly less root resorption than did the heavy force. The authors argued that the duration of force application appears to be an important factor in orthodontic root resorption. Even though the application of light orthodontic forces did not show a significant difference between 4 and 8 weeks of buccal force application, the amount of root resorption increased significantly from 8 to 12 weeks of force application. So the duration of orthodontic force application caused more root resorption even when light forces of 25 g were used. This finding agrees with others studies published by Vardimon et al. (1991) and Gonzales et al. (2008). Paetyangkul et al. (2011) affirmed that this might be due to the increased osteoclastic activity around 8 weeks of force application.
In another study, Chan and Darendeliler (2006) found that the mean volume of the resorption craters was 11.59 times greater in the heavy-force group than in the control group. Barbagallo et al. (2008), in a prospective randomized clinical trial compared forces applied with removable thermoplastic appliances (TA) and fixed orthodontic appliances. The results showed that teeth experiencing orthodontic movement had significantly more root resorption than did the control teeth. They also found that heavy force produced significantly more root resorptions (9 times greater than the control) than light force (5 times greater than the control).
In this context, Harris et al. (2006) conducted a prospective randomized clinical trial to quantify the amount of root resorption when controlled light and heavy intrusive forces www.intechopen.com

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were applied to human premolars and to establish the sites where root resorption is more prevalent. They found that the volume of the root resorption craters after intrusion was directly proportional to the magnitude of the intrusive force applied. The findings showed that the control group had fewer and smaller root resorption craters, the light force group had more and larger root resorption craters than the control group, and the heavy force group had the most and the largest root resorption craters of all groups. A trend of linear increase in the volume of the root resorption craters was observed from control to light to heavy groups, and these differences were statistically significant. The mean volumes of the resorption craters in the light and heavy force groups were 2 and 4 times greater than in the control groups, respectively. The mesial and distal surfaces had the greatest resorption volume, with no statistically significant difference between the 2 surfaces.

Direction of tooth movement
Evaluating the direction of tooth movement (intrusive vs. extrusive force), Han et al. (2005) found that root resorption from extrusive force was not significantly different from the control group. Intrusive force significantly increased the percentage of resorbed root area (4 fold). The correlation between intrusion or extrusion and root resorption in the same patient was r = 0.774 (P = 0.024).

Amount of apical displacement
In orthodontics, total apical displacement might represent a better marker for overall treatment activation. A tooth that is moved greater distances through bone is subjected to longer durations of activation. There is no way to move a tooth between two points with fixed appliances, without causing hyalinization. Perhaps, this is why maxillary incisors are most likely to exhibit severe levels of root resorption (Segal et al., 2004). Segal et al. (2004) conducted a meta-analysis to elucidate possible treatment-related etiological factors -such as, duration of treatment and apical displacement -for external root resorption and they found that mean apical root resorption was strongly correlated with total apical displacement (r = 0.822) and treatment duration (r = 0.852). In 2005, Fox also found that treatment-related root resorption is correlated with the distance the apex moves and the length of time the treatment took. Mandall et al. (2006) compared 3 orthodontic archwire sequences in terms of: (1) patient discomfort, (2) root resorption, and (3) time to working archwire. In that study, all patients were treated with maxillary and mandibular preadjusted edgewise appliances (0.022-in slot), and all archwires were manufactured by the same manufacturer. The results showed that there was no statistically significant difference between archwire sequences, for maxillary left central incisor root resorption (F ratio, P = 0.58). There was also no statistically significant difference between the proportion of patients with and without root resorption between archwire sequence groups (P = 0.8). Reukers et al. (1998) compared the prevalence and severity of root resorption after treatment with a fully programmed edgewise appliance (FPA) and a partly programmed edgewise appliance (PPA). All FPA patients were treated with 0.022-in slot Roth prescription (''A'' Company, San Diego, Calif), and misplaced brackets were rebonded. All PPA patients were treated with 0.018-in slot Microloc brackets (GAC, Central Islip, NY), and the archwires were adjusted for misplaced brackets. They found no statistically significant differences in the amount of tooth root loss (FPA, 8.2%; PPA, 7.5%) or prevalence of root resorption (FPA, 75%; PPA, 55%) between the groups.

Type of appliance
More recently, Scott et al. (2008) investigated the effect of either Damon3 self-ligating brackets or a conventional orthodontic bracket system on mandibular incisor root resorption. Patients were treated with Damon3 self-ligating or Synthesis (both, Ormco, Glendora, Calif) conventionally ligated brackets with identical archwires and sequencing in all patients. The results showed that mandibular incisor root resorption was not statistically different (Damon3, 2.26 mm, SD 2.63; Syn-thesis, 1.21 mm, SD 3.39) between systems. Brin et al. (2003) examined the effect of 2-phase vs 1-phase Class II treatment on the incidence and severity of root resorption. The results showed that children treated in 2 phases with a bionator followed by fixed appliances had the fewest incisors with moderate to severe root resorption, whereas children treated in 1 phase with fixed appliances had the most resorption. However, the difference was not statistically significant. As treatment time increased, the odds of root resorption also increased (P = 0.04). The odds of a tooth experiencing severe root resorption were greater with a large reduction in overjet during phase 2.

Genetic influences
Although several studies proved that there is a relationship between orthodontic force and root resorption, individual susceptibility also appears to influence the occurrence of root www.intechopen.com

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resorption. Since mechanical forces and other environmental factors do not adequately explain the variation seen among individual expressions of root resorption, interest has increased on genetic factors influencing the susceptibility to root resorptions (Hartsfield, 2009). The reaction to orthodontic force, including rate of tooth movement, can differ depending on the individual's genetic background (Abass & Hartsfield, 2007;Iwasaki et al., 2008).
In this context, pro-inflammatory cytokines like interleukin-1 (IL-1) and tumour necrosis factor (TNF) are known to induce synthesis of various proteins that, in turn, elicit acute or chronic inflammation. Al-Qawasmi et al. (2003) identified linkage disequilibrium between the IL-1B gene and root resorption in orthodontically treated individuals. The polymorphism variation was found to account for 15% of the variation in root resorption in that sample. Persons in their sample homozygous for the IL-1B allele 1 had a 5.6 fold (95 % CI 1.9-21.2) increased risk of root resorption greater than 2 mm as compared with those who are not homozygous for the IL-1 beta allele 1. Data indicate that allele 1 at the IL-1B gene, known to decrease the production of IL-1 cytokine in vivo (Pociot et al., 1992), significantly increases the risk of root resorption (Al-Qawasmi et al., 2003).

Systemic factors
A study conducted by Nishioka et al. (2006) determined whether there is an association between excessive root resorption and immune system factors. The prevalence of root resorption found was 10.3%. Allergy, abnormalities in root morphology and asthma showed be high risk factors for the development of excessive root resorption during orthodontic tooth movement. The modifying effect of several pharmacological agents on orthodontic root resorption also has been examined. Among them, L-thyroxine has been shown to have an inhibitory effect and clinical application has been attempted (Shirazi et al., 1999). Studies have been published describing anti-inflammatory properties of tetracyclines (and their chemically modified analogues) unrelated to their antimicrobial effect. A significant reduction in the number of mononucleated cells on the root surface was observed. Such cells have been related to root resorption (Mavragani et al., 2005).
Some authors have pointed that bone turnover has an important influence during orthodontic treatment. High bone turnover, found in patients with hyperthyroidism, can increase the amount of tooth movement compared with the normal or low bone turnover state and adult patients. Low bone turnover, found in patients with hypothyroidism, can result more root resorption, suggesting that in subjects where a decreased bone turnover rate is expected, the risk of root resorption could be increased (Verna et al., 2003). Bisphosphonates, potent inhibitors of bone resorption, causes a significant dose-dependent inhibition of root resorption in rats after force application. These results prompt that a thorough case history regarding possible pathophysiological conditions influencing bone metabolism should be performed on an individual patient basis. In subjects where increased bone turnover rates are expected, the reactivation of the appliance could be performed more frequently. However, in patients where decreased bone turnover rates are expected, the reactivation should be carried out less frequently and the risk of root resorption should be carefully evaluated (Verna et al., 2003(Verna et al., ). 1994Harris & Baker, 1990;Hendrix et al., 1994;McNab et al., 2000). One possible explanation for this could be the increased movement and retraction of the apex to close extraction spaces.
Another risk factor for severe root resorption is triangular roots (Marques et al., 2010). The geometric form of dental roots influences the distribution of forces on the alveolar bone and the dent al structure itself. Blunt roots and pipette-shaped apices (triangular) tend to concentrate the forces in a smaller area than roots with a normal shape (Marques et al., 2010). Most studies agree that pointed roots undergo resorption more frequently than those with normal shape (Hartsfield et al., 2004;Nigul & Jagomagi, 2006;Ng'ang'a & Ng'ang'a, 2003;Sameshima & Sinclair, 2001;Smale et al., 2005;Stenvik & Mjor, 1970).

How root resorption is repaired?
The transition of active root resorption into a process of repair is associated with the invasion of fibroblast-like cells from the circumference of the resorption crater into the active root resorption site even with a light force. The formation of new tooth-supporting structures is seen in the pheriphery of the resorption lacunae, whereas active resorption by multinucleated odontoclast-like cells took place in the central parts. When orthodontic force is discontinued, the reparative process is similar to early cementogenesis during tooth development (Brudvik & Rygh, 1995a, Brudvik & Rygh, 1995b. It has been suggested that the epithelial cell rests of Malassez might have a significant role in mediating repair cementogenesis (Brice et al., 1991;Hasegawa et al., 2003). The resorptive defects are repaired by the deposition of new cementum and the reestablishment of new periodontal ligament (Andreasen, 1973;Barber & Sims, 1981;Brice et al., 1991;Brudvik & Rygh, 1995b;Langford & Sims, 1982;Reitan, 1974).

Quality of research
Most of the studies cited in this chapter offer a low amount of scientific evidence and therefore do not yet allow the precise prediction of the interaction between orthodontic treatment, genetic/systemic factors and root resorption. Part of this insufficient evidence may be explained by the different methodological criteria employed, different sample sizes and the heterogeneity of the study populations. Thus, the findings have been conflicting, which compromises both the credibility and clinical application of the results. Also, the current state of knowledge does not allow orthodontists to identify which patients are vulnerable. In a recent systematic review, Weltman et al. (2010) stated that ''only 11 trials were considered appropriate for inclusion in this review, and their protocols were too variable to proceed with a quantitative synthesis. This reflects the state of the published scientific research on this topic.'' Furthermore, although severe root resorption can have drastic consequences to both treatment and patient health, there is only one study that specifically addresses the risk factors for this condition (Marques et al., 2010). The main factors directly involved in severe root resorption are extraction of first premolars, triangle-shaped roots and root resorption before treatment. In cases of extensive root resorption induced by orthodontic movement, there might be flaws in the predictability, prevention, and early diagnosis of this condition.
It is therefore important to determine the magnitude and prevalence of root resorption in various populations as well as related risk factors (Marques et al., 2010).
However, some challenging situations may appear to the orthodontist during orthodontic treatments. For example, in the study published by Marques et al. (2010), they found an excessive percentage of patients (6%) that experienced pauses in the mechanical treatment, there was a severe root resorption at the end of the treatment. This finding suggests the influence of genetic factors and further increases the responsibility of orthodontists with regard to this issue. If severe root resorption is identified, the treatment plan should be reassessed with the patient. Alternative options might include prosthetic solutions to close spaces, releasing teeth from active archwires if possible, stripping instead of extracting, and early fixation of resorbed teeth .

Care and recommendations
Determining the cause of root resorption requires a thorough medical history, including the past history of the tooth involved as well as vices, accidents, types of sports practiced, previous treatment and associated diseases. Relevant details, such as mild trauma (concussion and subluxation) should be analyzed in detail (Consolaro et al., 2011).
As root resorption is often asymptomatic, radiographic images constitute the best way to detect the condition and measure its severity in order to establish an early diagnosis (Eraso et al., 2007), especially control radiographs obtained after six to 12 months of orthodontic treatment (Artun et al., 2009;Weltman et al., 2010). Digital radiography (DR) and digital subtraction radiography (DSR) can be used for the detection of apical root resorption as small as 0.5 mm and lingual resorption of 1 mm or more. In this context, DSR frequently performs better than DR (Ono et al., 2011).
When an orthodontist identifies root resorption in a patient, the severity of the condition is decreased with a pause in active orthodontic movement for two to three months with a use of a passive archwire (Weltman et al., 2010;Zahrowski & Jeske, 2011). However, if the resorption is severe, the orthodontist and patient should reassess the treatment plan (Weltman et al., 2010). Alternative options include prosthetic solutions to close spaces, releasing teeth from active archwires when possible, stripping instead of extracting and early fixation of resorbed teeth . If root resorption is diagnosed on the final radiographs after treatment, follow-up radiographic examinations are recommended until the resorption has stabilized (Weltman et al., 2010). However, if it continues, sequential root canal therapy with calcium hydroxide may be considered (Pizzo et al., 2007).
There is little evidence that previous trauma (with no history of root resorption) and unusual tooth morphology play roles in increasing root resorption (Weltman et al., 2010). Caution should be used when retaining the teeth with fixed appliances, as occlusal trauma to the fixed teeth or segments may lead to extreme root resorption . As the magnitude of force has been documented to be directly correlated with the severity of root resorption (Casa et al., 2001;Darendeliler et al., 2004;Faltin et al., 2001;Harris et al., 2006), the ideal force for dental movement would mimic a physiologic balance between tooth movement and bone adaptation (Paetyangkul et al., www.intechopen.com Root Resorption in Orthodontics: An Evidence-Based Approach 437 2011). It is therefore recommended to employ light forces, especially for intrusive movements (Weltman et al., 2010).

Case report
The case described below illustrates an atypical situation, since with only four months of treatment using alignment and leveling wires (0.14 and 0.16), a severe root resorption was detected. This situation led the orthodontist to stop the orthodontic treatment. Fortunately, the case had low complexity and did not involve extensive tooth movements. In such cases, the orthodontist should be aware of the systematic radiological examinations.

Conclusions
While science provides no consistent evidence for the precise identification of the orthodontic patient that will develop root resorption, orthodontists should keep in mind the various indicators known and promote systematic radiographic to monitor their patients. Individualize the diagnosis and treatment plan could mean the difference between the success and failure of orthodontic treatment.