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Avi Shemesh,* DMD; Avi Levin, DMD; Joe Ben Itzhak, DMD; Yair Brosh, DMD; Evgeny Braverman, DMD; Gabriel Batashvili, DMD; and Michael Solomonov, DMD
Department of Endodontics, Israel Defense Forces (IDF) Medical Corps, Tel Hashomer, Israel
The purpose of this retrospective study was to identify the coexisting factors for EIR and to characterise EIR clinically and demographically. All cases of EIR that were referred to the endodontic department between 2011 to 2016 and diagnosed by an endodontist were evaluated. Demographic and clinical char-acteristics were collected and evaluated. Thirty-eight cases of EIR diagnosed between 2011 and 2016 were included in the study. Seventy-one percent of EIR cases were misdiagnosed by general practitioners. The most affected teeth were the maxillary central incisors (29% of cases) and mandibular molars (26%). Sixty-eight percent of EIR cases were diagnosed in teeth with clinically normal pulp. Pulp necrosis was observed mainly in the advanced stages (class 3 and class 4) of EIR (75%) and in teeth with a history of trauma (63%). Histo-ries of previous trauma and orthodontic treatment were reported in 29% and 23% of cases, respectively.
External Invasive Resorption (EIR) is a type of external resorption that features a narrow entry point of resorp-tion tissue mainly in the cervical area (1). Maxillary cen-tral incisors are the most frequently affected (1,2). EIR was described by Heithersay as a relatively uncommon form of external resorption. The clinical features vary from a small defect at the gingival margin to a pink coro-nal discoloration of the tooth crown (3).
EIR expands usually through the root, encircling the root canal without involving the pulp and resulting in a progressive loss of dental structure replaced by fibro-vas-cular tissue showing fibro-osseous features (1,3).
The pulp usually remains unperforated and healthy (uninflamed) due to the non-mineralied predentin layer (4,5). However, in long-standing lesions, the root canal may be perforated by the advancing resorptive lesion (3,6,7).
Heithersay classified EIR according to the extent of the lesion within the tooth (1). The distinctions include class 1, a small invasive resorptive lesion near the cervical area with shallow penetration into the dentin; class 2, a well-defined invasive resorptive lesion that has penetrated close to the coronal pulp chamber but shows little or no extension into the radicular dentin; class 3, a deeper invasion of dentin by resorbing tissue not only involving the coronal dentin but also extending at least to the coro-nal third of the root; and class 4, a large invasive resorp-tive process that has extended beyond the coronal third of the root canal (1).
Additional resorption channels are created beyond the main portal of entry of the resorption tissue in cases with advanced lesions. The channels burrow deeply into the dentin and later interconnect more apically with the peri-odontal ligament by communicating channels (3).
The radiographic features of EIR may vary from the well-defined to an irregular bordered mottled radiolu-cency that sometimes overlies the outline of the pulp space, whereas the canal contour remains distinct (3).
The exact reason for EIR is unknown to this day, but Heithersay described a few potential predisposing factors including orthodontic treatment (21.1%), trauma (15%), intracoronal bleaching (3.9%), a combination of trauma and bleaching (7.7%) and a combination of trauma, bleaching and orthodontic treatment (1.8%) (1). Other studies supported the claim that EIR might be a complica-tion of traumatic injury after orthodontic tooth movement, dento-alveolar surgery, periodontal treat-ment or bleaching (2,6,7).
The purpose of this study was to investigate the possi-ble coexisting factors and demographic and clinical char-acteristics of EIR.
The study protocol was reviewed and approved by the Ethics Committee of Medical Corps, IDF (IDF-1684).
All patients who were examined and received EIR diagnoses in the Department of Endodontics, Israel Defense Forces (IDF) Medical Corps, Tel Hashomer, Israel, between 2011 and 2016 were included in this study.
The data from each patient examination, including demographics and clinically relevant information, were collected and documented. Demographic data included gender, age and referral cause. Clinical findings included the involved tooth, pulp diagnosis, discoloration, probing depth, symptoms and cavitation that related to EIR. Pos-sible coexisting factors included trauma, orthodontic treatment and bleaching. Clinical findings included –
Resorption stage was determined based on radio-graphic evaluation according to Heithersay’s classifica-tion. Diagnostic radiographs from the examination were re-evaluated by two endodontists with EIR experience (A.S., A.V.) who simultaneously judged the bite-wing and peri-apical radiographs for each case. They simulta-neously analysed each case to reach a consensus for the interpretation of the degree of the resorption. The radio-graphs were viewed in a magnification device with an inbuilt light source in a room with dimmed light.
All of the possible coexisting factors, demographics and clinical characteristics and findings were summarised and evaluated.
A total of 38 cases of EIR were diagnosed between 2011 and 2016. All cases were referred by general practition-ers. Eleven (29%) cases were referred with possible EIR diagnoses. In the other cases, the referral causes were un-identified resorption or internal resorption. EIR was diag-nosed in all groups of maxillary teeth and in mandibular molars and premolars. The most frequently affected teeth were central incisors (11 cases - 29%) and mandibular molars (12 cases - 26%). EIR was diagnosed mainly between the ages of 18 and 30 (29 cases - 76%). Seven cases (19%) were diagnosed between age 31–40 and two cases (5%) between age 41–50.
Twenty-three (87%) cases were diagnosed in advanced stages of EIR (stages 3 and 4 according Heithersay’s classi-fication). Most of the cases (69%) of EIR were diagnosed in teeth with clinically normal pulp.
Sixteen (84%) cases of class 3 EIR involved teeth with clinically normal pulp, whereas seven (50%) of the class 4 EIR cases were clinically normal pulp (Table 1). IER was diagnosed also in teeth with pulp necrosis and endodontically treated teeth. The distribution of cases according Heithersay classification is shown in Table 1.
Table 2 presents the clinical findings according to dif-ferent pulp diagnoses. Thirteen (34%) cases had evidence of crown discoloration, 12 of which were pink discol-oration and one grey (tooth with pulp necrosis). Cavita-tion and periodontal pockets greater than 3 mm in size were detected almost quarter of cases.
Eight (21%) cases had previous orthodontic treatment, 10 (26%) had previous trauma to the involved teeth and one case (3%) had a combination of trauma and orthodontic treatment. Eight (89%) of the cases with pre-vious orthodontic treatment had clinically normal pulp, whereas only four (36%) of the teeth with previous trauma had clinically normal pulp (Table 3).
EIR was described in the literature by Tronstad and Ne and was comprehensively investigated by Heithersay (1,3,6–8) in the 1990s. His articles described the possible predisposing factors and demographic, clinical and radio-graphic characteristics of external invasive resorption.
EIR occurred in all tooth groups, except the mandibu-lar incisors and canines, and was observed most fre-quently in the central maxillary incisors followed by the mandibular molars. Heithersay found that maxillary inci-sors, maxillary canines and mandibular molars were the teeth most frequently affected (1). Mavridou et al. (2) 2017 found that most ECR cases were observed on maxillary central incisors followed by maxillary canines and mandibular molars. Other studies have described EIR in maxillary and mandibular molars, maxillary and mandibular premolars and maxillary incisors and canine (9–13).
Table 1 Pulp diagnosis of the teeth in different stages of EIR
|Total||Clinically normal pulp||Pulp necrosis||Endodontically treated tooth|
|Class 2||5||3 (60%)||2 (40%)||0|
|Class 3||19||16 (84%)||1 (5%)||2 (11%)|
|Class 4||14||7 (50%)||5 (36%)||2 (14%)|
|Total||38||26 (68%)||8 (21%)||4 (11%)|
Table 2 Clinical findings in different pulp diagnosis
|Total||Discoloration||Symptoms||Cavitation||Deep pocket >3 mm|
|Clinically normal pulp||26||8 (30%)||1 (4%)||6 (6%)||6 (23%)|
|Pulp necrosis||8||4 (50%)||1 (13%)||2 (24%)||1 (13%)|
|Endodontically treated tooth||4||1 (25%)||0||0||3 (75%)|
|Total||38||13 (34%)||2 (5%)||8 (21%)||10 (26%)|
Table 3 Coexisting factors in different pulp diagnosis
|Clinically normal pulp||26||8 (30%)||4 (15%)||0|
|Pulp necrosis||8||1 (12%)||5 (63%)||0|
|Endodontically treated tooth||4||0||2||0|
|Total||38||9 (23%)||11 (29%)||0|
In the present study, EIR was diagnosed mostly between 18 and 30 years old (76%) while a percentage of between 8% and 14% was observed for different age groups above 15 up to 54 years in other study (2). The difference in the present study is caused by the age distri-bution of the patients in the dental clinic of the Israel Defense Forces Medical Corp. Therefore, the age distribu-tion that was found in the present study is not represen-tative of the entire population.
In the present study, EIR was diagnosed mainly in clin-ically normal pulp teeth (26 cases) (Table 1). Eight cases were diagnosed in teeth with necrotic pulps and four cases in endodontically treated teeth (Table 1). EIR encir-cling the root canal and the pulp usually remains unper-forated and healthy (uninflamed) due to the presence of a non-mineralised predentin layer (3–6). However, in long-standing lesions, the root canal may be perforated by the advancing resorptive lesion (3,6,7). Therefore, in the 34 teeth without previous endodontic treatment, most cases of EIR involved teeth with clinically normal pulp. Five of the eight cases of the teeth with pulp necro-sis had previous trauma, and six of these eight cases were EIR stage 4. The two cases of pulp necrosis that were EIR stage 2 had previous trauma. Therefore, the pulp necrosis may be explained by previous trauma or by the advanced stage of EIR.
Although the history of symptoms, clinical and radio-graphic findings at the time of the endodontic treatment in the four cases of EIR in endodontically treated teeth is missed, it is possible that the root canal treatment may be explained by doing root canal treatment in these teeth due to misdiagnosis by general practitioners.
The radiographic features of EIR may vary from the well-defined to an irregularly bordered mottled radiolu-cency, sometimes overlying the outline of the pulp space, while the canal contour remains distinct (3). Recently, a new three-dimensional classification of EIR was pub-lished . In the present study, all cases were classified according Heithersay’s classification because the new classification was published after data collection was done (14). Moreover, size and nature of EIR on radio-graphs are underestimated in comparison to Cone Beam Computed-Tomography (15). In the present study, from all diagnosed EIR cases, based on radiographs, five cases were class 2, 19 cases were class 3 and 14 cases were class 4 (Table 1). Class 1 was not diagnosed presumably because EIR is difficult to diagnose in the early stage, and general dentists are not familiar with EIR. Therefore, in the present study, general practitioners accurately diag-nosed only 29% of cases, and the causes for referral in the other cases were not related to EIR. EIR diagnosis by general practitioners may be widely improved by intro-ducing this population to the clinical, radiographic and demographic characteristics of EIR.
In the present study, eight (21%) cases involved deep periodontal pockets in the resorption area (Table 2). Peri-odontal pockets appear in EIR cases because the resorp-tion includes the adjacent alveolar bone. An infrabony periodontal pocket may be identified even in radiographs
(6). Thirteen (34%) cases had crown discoloration. Twelve cases (one case with EIR class 2, five cases with EIR class 3 and six cases with EIR class 4) had pink discol-oration of the crown, whereas one case of a tooth with pulp necrosis had grey discoloration. The pink discol-oration of the crown appears in advanced stages because the well-vascularised granulation tissue reaches the supra-gingival area of the crown and may be visible through the enamel (3,6).
Thirty-six cases (95%) of the teeth with EIR were asymptomatic while two cases were diagnosed with irre-versible pulpitis. Although the presence of the predentin was not investigated in this study, the finding that most of the EIR cases were not symptomatic may be explained by the presence of the non-mineralised predentin layer to protect the pulp that stays healthy (4,5).
In the present study, the possible connection between EIR and the main coexisting factors – previous orthodon-tic treatment, traumatic injury and bleaching was investi-gated (Table 3). More than half of the cases had previous traumatic injury or orthodontic treatment. One case (3%) had a combination of trauma and orthodontic treat-ment while none of the cases had previous internal bleaching (Table 3). In an analysis of 222 patients (257 teeth) referred for treatment, it was found that a history of orthodontic treatment was the most common sole pre-disposing factor for a tooth to develop EIR, followed by trauma and intracoronal bleaching (1). Tronstad (1988) claimed that EIR might be a complication of traumatic injury after orthodontic tooth movement, dento-alveolar surgery, periodontal treatment or bleaching (6). Ne (1999) claimed that EIR might follow injuries such as tooth trauma, surgical procedure, orthodontic treatment, bruxism, bleaching and periodontal root planning and scaling (7). Mavridou found that in 59% of the cases, more than one potential predisposing factor was identi-fied and that the most frequently appearing factor was orthodontics followed by trauma (2). However, the occurrence rate of EIR in orthodontic patients is not known. In a post-orthodontic follow-up study, EIR was diagnosed in one incisor in 87 patients (16). In another publication that studied the occurrence of cervical inva-sive root resorption in the first and second molar teeth of orthodontic patients, EIR had a low mid-term (5%) occurrence (9). A recent study found that application of a 1 N force over a 2-month period provokes severe root resorption at the compression cervical sites (17).
The occurrence of EIR after internal bleaching was related to the old internal bleaching technique that was based on 35% hydrogen peroxide (Superoxol) (18). In the past 15 years, sodium perborate has been used for internal bleaching in Israel dentistry instead of hydrogen peroxides. This may be the reason that none of EIR cases described occurred after internal bleaching. The results regarding the percentages of EIR cases that had histories of previous orthodontic treat-ment or trauma are similar to those of previously pub-lished studies, but the link between EIR and these factors may be circumstantial.
In conclusion, EIR may appear in nearly any group of teeth, especially in maxillary central incisors. EIR appears in patients mostly between 18 and 30 years old and occurs more frequently in men than women. The pulp is usually clinically normal pulp and may be accompanied by crown cavitation, pink crown discoloration or deep periodontal pockets. Fifty percent of cases are idiopathic without coexisting factors, such as previous orthodontic treatment, traumatic injury or internal bleaching. A cir-cumstantial link between EIR and the coexisting factors such as orthodontic treatment and traumatic injury should be further investigated.
All authors have contributed significantly and all authors are in agreement with the manuscript.
The authors have no conflicts of interest to declare.