MR.

SHANON PATEL (Orcid ID : 0000-0003-0614-6951)

Article type : Review

Accepted Article
External cervical resorption-part 1: Histopathology, distribution, and presentation.

Patel S1,2, Mavridou A3, Lambrechts P3, Saberi N1

1
Department of Endodontology, King’s College London Dental Institute, London, UK,
2
Specialist Practice, London, UK, 3Department of Oral Health Services, University of Leuven,

Leuven, Belgium.

Running Head: External cervical resorption-part 1

Key words: external cervical resorption, histology, nano-CT, cone beam computed

tomography

Correspondence:

Dr. Shanon Patel

Department of Endodontology, Kings College Dental Institute, Floor 25 – Tower Wing, Guys

Hospital, London SE1 9RT, UK

e-mail: shanonpatel@gmail.com

Abstract

External Cervical Resorption (ECR) is the loss of dental hard tissue as a result of

odontoclastic action. It is a dynamic process that involves periodontal, dental and in later

stages pulpal tissues. Over the last two decades ECR has attracted increased interest, this

is in part due to novel micro-CT and histopathological techniques for its assessment, and

also improved radiographic detection using CBCT. This literature review will cover the

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 aetiology, potential predisposing factors, histopathology and diagnosis of ECR. Part 2 will

cover the management of ECR.

Accepted Article
Introduction

Root resorption is the loss of dental hard tissue (i.e. cementum, dentine and/or enamel) as a

result of odontoclastic action (Patel et al. 2009a). Root resorption is desirable in deciduous

teeth (physiological root resorption) as it facilitates their exfoliation, and subsequent eruption

of the underlying permanent successor tooth. Root resorption in adult teeth is undesirable as

it leads to irreversible damage, which may necessitate dental treatment, or even extraction.

Root resorption may be simply classified by its location on the root surface as external or

internal resorption. External root resorption may be further sub-classified into surface

resorption, external inflammatory resorption, external cervical resorption, external

replacement resorption and transient apical resorption (Patel & Pitt Ford 2007). External

cervical resorption (ECR) usually manifests in the cervical aspect of teeth; it develops as a

result of damage to, and/or deficiency of the periodontal ligament (PDL) (Andreasen &

Andreasen 2007) and the subepithelial cementum.

External cervical resorption (ECR) is a dynamic process that involves periodontal, dental

and in later stages pulpal tissues (Luso & Luder 2012, Mavridou et al. 2016a), and has

attracted increased interest in the last two decades (Thönen et al. 2013, Mavridou et al.

2017a). This is due to a combination of improved radiographic detection with CBCT (Patel et

al. 2007, 2009b, Durack et al. 2011), and novel micro-CT and histopathological assessment

of ECR (Mavridou et al. 2016a,b, 2017b).

An electronic literature search was carried out and included the databases Medline (Ovid),

PubMed and Embase. The cut-off date was set to October 2017. However, complementary

searches were also carried out in November and December 2017. The searches used

controlled vocabulary and free-text terms. These included the terms ‘root resorption’, ‘tooth

resorption’, ‘external cervical resorption’, ‘invasive cervical resorption’, ‘peripheral cervical

resorption’, ‘extracanal invasive resorption’, ‘odontoclastoma’, ‘peripheral inflammatory root

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 resorption’, ‘supraosseous extracanal invasive resorption’, ‘idiopathic external resorption’

and ‘ECR’. In addition to database searches, the ‘early view’ and prepublication online
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sections of major international journals were also individually checked.

The articles were reviewed independently by two evaluators (NS and SP) for their relevance

in terms of overall scientific evidence for ECR. In addition, the reference lists of these

articles were reviewed to identify any relevant studies that had not been identified via

previous electronic or hand searches. Overall 147 articles were assessed.

The review of literature revealed the lack of original basic scientific research papers on the

subject of ECR. While there are many published articles on the topic, the majority of these

are case reports, case series, treatment demonstrations or narratives (Table 1), which lack

adequate scientific quality as described by Centre for Evidence-based Medicine (CEBM) and

their hierarchical system. Although it has been generally recognized that the best clinical and

scientific evidence is a combination and amalgamation of clinically relevant research and

individual clinical expertise (Sackett et al. 1996), in the case of ECR, the evidence of the

former is sparse.

This lack of evidence may be attributed to treatment-focused nature of many of the previous

publications, as opposed to an enquiry-based practice. This has resulted in the lack of

understanding of the true nature of ECR, which could potentially lead to misdiagnosis (and

potential under-reporting) and mismanagement of ECR.

This review would ideally take the form of a systematic review of randomised controlled

trials. However, this is not possible as majority of literature on this topic, as explained and

demonstrated above, consists of case (series) reports, review papers and ex vivo studies

thus making such a review impossible to perform. The aim of part 1 of this literature review

is to present the relevant literature on the aetiology, pathogenesis and diagnosis, part 2 will

describe the management of ECR.

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 Aetiology

Although several potential aetiological factors have been associated with the development
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and progression of the ECR, the aetiology and pathogenesis of ECR is still poorly

understood and as a result many of these resorptive defects are misdiagnosed, under-

reported and mismanaged.

Heithersay (1999b) assessed 257 teeth with ECR and postulated that orthodontic treatment,

traumatic injury, internal bleaching, surgery and restorative treatment were the principle

potential predisposing factors for ECR. Mavridou et al. (2017a) assessed 337 ECR cases

and reported several additional potential predisposing factors; several of which had

previously been identified in case (series) reports (Figure 1). These included extraction of a

neighbouring tooth (Gunst et al. 2013), malocclusion (Vossoughi & Takei 2007), playing

wind instruments (Gunst et al. 2011), periodontitis (Beertsen et al. 2001), autotransplantation

(Kandalgaonkar et al. 2013), transmission of feline viruses to humans (von Arx et al. 2009),

herpes zoster (Solomon et al. 1986, Ramchandari & Mellor 2007, Patel et al. 2016a),

systemic and genetic factors (Moskow 1989, Llena-Puy et al. 2002, Edwards & McVaney

2005, Neely & Gordon 2007, Arroyo-Bote et al. 2017), the use of bisphosphonates (Patel &

Saberi 2015), impacted teeth (mandibular third molars affecting mandibular second molars,

spontaneous resorption of impacted teeth), cysts, tumours (Fuss et al. 2003) and pressure

of erupting canines applied to lateral incisors (Ericson et al. 2002, Alqerban et al. 2009,

Halder-Olsen et al. 2015).

Orthodontic treatment as a potential predisposing factor increased from 28.4% (Heithersay

1999b) to 45.7% (Mavridou et al. 2017a). This increased incidence may be partly attributed

to increased awareness of ECR (Chen et al. 2010), and increased uptake of orthodontics

treatment (RIZIV 2017).

The decreased incidence of internal bleaching as a potential predisposing factor as reported

by Mavridou et al. (2017a) may be due to milder bleaching products being used nowadays

compared to concentrations of 30% H2O2 used in the past (Friedman et al. 1988, Rotstein et

al. 1991, Attin et al. 2003). However, even with this reduced concentration of bleaching

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 agents, diffusion of hydroxyl radicals can damage the PDL fibroblasts (Rotstein et al. 1993,

Chapple & Matthews 2007, Lou et al. 2016). Therefore, it is essential to advise patients of
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potential risk for ECR, especially when performing bleaching on younger patients, as the

diameter of their dentinal tubules is larger and the risk for diffusion is greater (Camps et al.

2007).

Marvidou et al. (2017a) reported only a 1.2% association with restorative procedures,

compared to 14.4% reported by Heithersay (1999b).

In the veterinary literature, ECR is referred to as Feline Odontoclastic Resorptive lesions

(FORL) or Tooth Resorption (TR). The prevalence has been reported to vary significantly

from 14.3%-85%, depending on the examined cat populations and the different experimental

methodology used (Pettersson 2010). Von Arx et al. (2009) first suggested that the

transmission of Feline Herpes Virus (FHV) can result in multiple human ECR lesions. It has

been suggested that FORL is a multifactorial condition in which bacterial and/or viral

infections trigger an inflammatory process that subsequently leads to FORL initiation (Booij-

Vrieling 2010). The possibility of virus transmission from cats to humans and its impact on

ECR initiation needs further investigation.

Traumatic injuries in particular luxation and avulsion result in localized damage and/or

rupture of PDL; this has also been suggested as a cause of ECR (Heithersay 1999b, Trope

2002, Andreasen & Andreasen 2007, Mavridou et al. 2017a).

Other researchers have also suggested that bacteria-induced inflammation may be involved

in ECR (Beersten et al. 2001, Lin et al. 2013).

In the majority (59%) of clinical cases (199/337 teeth), more than one potential predisposing

factor was identified, indicating that ECR is multifactorial and not idiopathic (Mavridou et al.

2017a). Some combinations of potential predisposing factors such as orthodontics with

traumatic injury (17.6%) (19/108 teeth), with parafunctional habits (13%) (14/108 teeth) or

extraction of a neighbouring tooth (12%) (13/108 teeth), have a much higher frequency

suggesting a multifactorial aetiology. It should be mentioned that in previous reports only

20% of the ECR cases were identified as multifactorial (Heithersay 1999b). This difference is

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 believed to be due to the establishment of a more systematic experimental approach

(Mavridou et al. 2016b) and to the consideration of an updated list of potential predisposing
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factors (Mavridou et al. 2017a).

Histological and 3D characteristics of ECR

ECR cases share several common features (Heithersay 1999a, Luso & Luder 2012,

Mavridou et al. 2016a). These are; (a) the initiation point (portal(s) of entry), (b) the

resorption area with its channels and external interconnections (portals of exit), (c) the

Pericanalar Resorption Resistant Sheet (PRRS), (d) the repair by substitution of the

resorbed tissues by reparative bone-like tissue and finally (e) the remodeling of this

reparative tissue (Mavridou et al. 2016a). In root filled treated teeth there is no PRRS area

due to its removal during the mechanical preparation of the root canal (Mavridou et al.

2017b).

(a) Portal(s) of entry: Are located in the cementum below the gingival epithelial

attachment. This area has typically two histological patterns (Mavridou et al.

2016a). Firstly, a connective tissue with a dense inflammatory lymphoplasmacytic

infiltrate, epithelial tissue is often seen to cover the granulation tissue (Figure 2)

(Lin et al. 2013, Mavridou et al. 2016a). Secondly, an ingrowth of reparative

bone-like tissue occurs, while local fusion of the adjacent alveolar bone with

resorbed dentine and even resorbed enamel occurs. In any case, the localised

destruction and/or removal of PDL at the portal of entry is needed for ECR to

occur (Karring et al. 1980, Nyman et al. 1980, Mavridou et al. 2016a) (Figure 3).

(b) Resorption area containing channels and external interconnections:

Resorptive lesions expand in all 3 dimensions away from portal(s) of entry encircling

and/or progressing towards the root canal system, resulting in the destruction of

dental hard tissues (i.e. cementum, dentine and enamel). Several resorption

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 channels and interconnections with the PDL (portals of exit) are created. The

advancing resorptive lesion is prevented from perforating into the root canal by the
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Pericanalar Resorption Resistant Sheet (PRRS see below).

Resorption (clastic) cells located within resorption lacunae (von Arx et al. 2009), are

identified as large osteoclast-like multinucleated cells with a size of approximately 20

x 30 μm (Mavridou et al. 2016a) (Figure 4). When the clastic cells are detached,

other types of cells (mononuclear phagocytes, or osteoblast-like cells entrapped in

osteoid) can repopulate the lacunae area (Mavridou et al. 2016a).

(b) Pericanalar resorption resistant sheet (PRRS): Is a non-uniform layer/area

with a thickness of 70 up to 490 μm depending on its location within the root

(Mavridou et al. 2016a) (Figure 5). Histological and micro-CT assessment has

confirmed that the PRSS consists of dentine and occasionally bone-like tissue

(Gunst et al. 2013, Mavridou et al. 2016b) (Figure 6). Although the term ‘resistant’

is used, pulp perforation can occur especially in advanced cases. In areas with

small PRRS disruptions, the cellular consistency of the pulp is modified and

odontoblasts can be atrophic (Figure 6a). In other areas of the pulp, the

odontoblastic layer appears intact (Figure 6a). Histological findings also include

the formation of pulp stones and diffuse calcifications (Figure 6b). Other

observations included hyalinosis (thickening of the walls) of the blood vessels

and an increase of the deposition of predentine (Mavridou et al. 2016a).

(d) Repair: Repair of the resorbed dental hard tissues occurs by ingrowth and

apposition of reparative bone-like tissue through the portal(s) of entry into the tooth

(Figure 7, 7a, 7b). The reparative tissue appears as a lamellar trabecular bone, with

islands of woven bone formed in regions of rapid bone repair-remodelling cycle.

Histological findings show bone-like related cells (Osteoblast-like cells, osteocytes)

and osteoid tissue (Mavridou et al. 2016a) (Figure 3).

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 (e) Remodelling of reparative bone-like tissue; Remodelling refers to the cyclic

resorption and reforming of the bone-like tissue involving clastic and blastic cells. It is
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possible that in different areas of the same tooth active resorption of dentine, active

repair by osteoid formation and remodelling of the bone-like tissue take place

simultaneously (Mavridou et al. 2016a) (Figure 6).

Pathogenesis

ECR is a dynamic and evolving process, with destructive and reparative phases (Luso &

Luder 2012, Mavridou et al. 2016a). The pathogenesis of ECR consists of three main

stages:

Resorption initiation: This is the first stage of ECR and is characterized by a localised

destruction/disruption of the normal PDL structure, including the unmineralized cementum

leading to the formation of a blood clot and a localised inflammatory response of the

exposed dentine (Polimeni et al. 2006). Macrophages then migrate to the affected area and,

in addition to wound debridement, will result in the formation of granulation tissue (Karring et

al. 1980). The granulation tissue is also able to contact the dentine through an exposure in

the cementum-enamel junction (CEJ). This ‘gap’ may be either due to a localized cementum

removal, caused by traumatic damage or a cemental tear (Lin et al. 2011) or due to a natural

incomplete closure of cementum over enamel in this area (Schoerder & Scherle 1988,

Neuvald & Consolaro 2000). Thus, the exposed dentine could be vulnerable to resorption

from the adjacent bone or to circulating immune cells which are attracted to the underlying

mineralized dental hard tissue. Different types of the cells (bone, PDL fibroblasts or epithelial

gingival cells) can repopulate the wounded area and different phenomena may occur

(Nyman et al. 1985). In the case of bone cells, ankylosis can occur (Melcher 1970, Line et al.

1974, Nyman et al. 1980). In the case of PDL cells, cementum formation and PDL

regeneration will take place (Melcher 1970, Line et al. 1974, Karring et al. 1980). In case of

epithelial gingival cells, no repair will take place (Nyman et al. 1980). The stimulation of

clastic cells is mainly through the expression of ‘Receptor Activator of Nuclear Factor k B

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 Ligand’ (RANKL) by clastic cells, damaged and compressed periodontal ligament cells

and/or certain bacterial species. RANKL binds to RANK receptors of clastic precursor cells,
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which will then become mature clastic cells by means of fusion (Kanzaki et al. 2001,

Fukushima et al. 2003, Belibasakis et al. 2007, Uchiyama et al. 2009).

Recent evidence suggests that hypoxia also might play a role in the activation of

osteoclastogenesis (Knowles & Athanasou 2009), as it can disturb the metabolism and

impede the recovery of human periodontal ligament fibroblasts (Zhang et al. 2013). The

synergetic effect of hypoxia and bacteria in the PDL may also accelerate the inflammation

(Gölz et al. 2015).

Resorption progression: Several factors have been suggested as stimulating factors for ECR

to progress. These include; infection (bacteria) (Gölz et al. 2015, Mavridou et al. 2016a),

continuous mechanical force on the PDL (e.g. during orthodontic treatment) (Niklas et al.

2013, Le et al. 2016), discontinuous mechanical unloading (Arnett et al. 2003) caused by

chewing, parafunction or a combination. All these factors may induce a hypoxic

microenvironment, which activates osteoclastogenesis (Arnett et al. 2003, Knowles &

Athanasou 2009, Arnett 2010) and subsequently helps in the progression of ECR (Mavridou

et al. 2017a). Hypoxia as a driving force of angiogenesis could influence the continuous

development of highly vascularized granulation tissue accompanying ECR (Mavridou et al.

2016a, Rombouts et al. 2017).

In this phase the resorptive process invades the tooth structure by resorbing cementum,

dentine and enamel (Mavridou et al. 2016a). The resorptive lesion extends in all planes (i.e.

circumferentially and longitudinally) within the dentine. The direction that clastic cells move

in is dependent on inflammatory mediators (e.g. growth factors, cytokines, prostaglandins

etc.) and hormones (e.g. parathyroid hormone (PTH), calcitonin, 1,25-dihydroxyvitamin

D3 (calcitriol) (Manolagas 2002, Väänänen 2005). The presence of the PRRS helps to

prevent ECR from perforating into the root canal, thus the pulp tissue retains its vitality

(Mavridou et al. 2016a). It has been suggested that the PRRS includes an inhibitory

resorptive factor (Wedenberg 1987) and lacks RGD proteins (Levin 2012) which make it

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 resistant to resorption. However, in advanced cases of ECR the root canal may become

perforated.
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Reparative stage: This is the reversed stage of ECR, where repair takes place by

osteoblast-like cells that result in an ingrowth of bone-like tissue into the resorption cavity

(Mavridou et al. 2016a). The reparative tissue and the tooth structure eventually become

part of the normal alveolar bone structure (Levin 2012). This is regarded as a form of

healing. After formation of the bone-like tissue, active remodeling can occur asynchronously

at many sites. During this stage, repair and remodeling evolve simultaneously at different

areas of the tooth (Mavridou et al. 2016a, 2017b). This phenomenon is responsible for

changes in the CBCT image in long term follow up of ECR.

Distribution

ECR is most commonly detected in maxillary central incisor teeth. Heithersay (1999b) and

Mavridou et al. (2017a) detected ECR in 29.2% and 28.8%, respectively, in 257 and 337

teeth which were diagnosed with ECR (figure 8).

The next most affected teeth were maxillary canine, maxillary lateral incisor, mandibular first

molar and maxillary first molar teeth. The incidence of ECR was in the same order of

magnitude in both studies (Heithersay 1999b, Mavridou et al. 2017a). This similar pattern of

tooth distribution in these studies may be associated with the high prevalence of traumatic

injuries (anterior teeth) (Bastone et al. 2000) and parafunctional habits (molar tooth) in

patients (Chatzopoulos et al. 2017). In another study which assessed all ECR cases with

radiographs and CBCT, the incidence was similar for maxillary central incisor teeth (30.4%),

however, the next common teeth were mandibular first molar, mandibular central incisor and

maxillary molar teeth (Patel et al. 2016b).

The increased incidence of ECR in premolar teeth in the study of Mavridou et al. (2017a)

may be associated with the increased uptake of orthodontic treatment (e.g. extraction of the

first premolar and orthodontic movement thereafter).

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 Mavridou et al. (2017a) detected ECR more frequently in younger age groups than reported

by Heithersay (1999b). This may be due to a combination of factors including; increased

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uptake of orthodontic treatment, increased visits to general dentists for check-ups and more

awareness of the clinical and radiographic appearance of ECR (Proffit et al. 2013, Van der

Heyden 2013, RIZIV 2017). ECR does not seem to be related to the gender of the patient

(Heithersay 1999b, Mavridou et al. 2017a).

Heithersay (1999b) and Mavridou et al. (2017a) provided detailed and extensive descriptions

of the potential aetioloigcal factors of ECR. However, it must be stressed that no definitive

cause-and-effect relationship has been established. In the cases affected by a combination

of predisposing factors, it was impossible to determine definitively whether ECR was the

result of one specific event or a combination of factors, or if any of the potential causes

identified were in fact contributory. In 15% of the patient examined in Heithersay’s study, no

potential predisposing factor was identified, furthermore, intracoronal restorations were

attributed as possible predisposing factors only when no other potential cause could be

identified (Heithersay 1999b, Patel et al. 2016).

Clinical presentation

Patients commonly are asymptomatic and therefore ECR may be diagnosed purely as an

incidental clinical and/or radiographic finding. In more advanced cases, when the resorption

lesion has affected the pulp, the patient may present with symptoms of (ir)reversible pulpitis

and/or apical periodontitis (Figures 9-11).

The diagnosis of ECR defects can be challenging (Gulabivala & Searson 1995, Schwartz et

al. 2010, Durack & Patel 2016, Patel et al. 2017). The clinical presentation of ECR defects is

determined by their location and nature. While early defects or those located in interproximal

aspects of teeth may not be readily detected on clinical examination, extensively cavitated

cervical defects on the labial or lingual areas may be diagnosed by direct vision or detected

upon probing with dental probes or periodontal scalers (Bergmans et al. 2002, Patel et al.

2009a, 2016). These defects bleed profusely on probing as a result of their vascularity

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 (Trope 2002, Patel et al. 2009a). Due to their location, ECR may be mistaken for buccal

caries, therefore it is important to differentiate these lesions by tactile feedback (probing).

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Depending on its state, caries will feel soft or sticky on probing, whereas ECR will be hard

and scratchy (Bergmans et al. 2002, Patel & Pitt Ford 2007, Patel et al. 2009a).

A ‘pink’ spot or banding in the cervical aspect of the tooth is usually pathognomic of ECR

(Heithersay 2004, Patel & Pitt Ford 2007). The discoloration is due to the fibrovascular

granulation tissue within the resorptive defect being visible through the thinned-out overlying

enamel (Bergmans et al. 2002). As described above, this highly vascular granulation tissue

is the reason behind its profuse bleeding on probing. Although pink spots may be easily

detected by the patient and/or clinician, they are more challenging to detect on posterior

teeth, especially when they are located on the interproximal or lingual/palatal aspects of the

tooth (Figure 11). It must be stressed that pink spots are relatively rare. Teeth with ECR may

also be discoloured due to pulp necrosis; in these cases they will show a grey discolouration

(Figure 7).

As there is no classic presentation of ECR, many defects may present as incidental signs on

clinical or radiographic examination or as a result of pulpal involvement, i.e. symptoms of

(ir)reversible pulpitis (e.g. temperature sensitivity), or in more advanced cases they may be

infected and display signs of apical periodontitis (e.g. tenderness to percussion, presence of

a sinus) (Bergmans et al. 2002, Patel et al. 2009a, Bhuva et al. 2011). Teeth affected by

ECR respond positively to sensibility testing as long as the root canal has not been

perforated and the pulp became necrotic (Frank & Torabinejad 1998, Patel et al. 2009a).

In the co-author’s experience, early ECR lesions are being more commonly detected by

hygienists who purposefully, as part of their treatment visually assess and gently probe and

scale the circumference below, and above the CEJ of their patient’s teeth.

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 Radiographic presentation

There is no ‘classic’ radiographic appearance of ECR. Lesions may be symmetrical or

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asymmetrical, their margins vary from being well defined and smooth to poor definition or

ragged or even with no clear delineation between ECR and healthy root structure (Durack &

Patel 2016).

ECR in the ‘resorptive’ phase will be radiolucent in nature, whereas ECR lesions in the

‘reparative’ phase will be more radiopaque, i.e. a mottled or cloudy appearance as a result of

the ossification of the granulomatous resorptive tissue (Figure 12). In some cases, there

may also be distinct, radiopaque striations of hard tissue present (Iqbal 2007, Gunst et al.

2013).

The outline of the root canal walls should be intact and traceable through the lesion; this

distinguishes it from internal inflammatory resorption. The parallax imaging technique may

be used to distinguish between internal resorption as well as confirm the location of ECR

lesions which are not clinically detectable. The canal walls will be visible with horizontal

parallax radiographs, however, the ECR lesion will appear to move with the change of

horizontal angle of the X-ray tube. Lingualy/palataly located ECR will appear to move in the

same direct as the parallax shift, whereas labially/buccally located ECR will appear to move

in the opposite direction to the X-ray tube shift. Internal root resorption lesions will always

stay centered with parallax radiographs (Durack & Patel 2016).

Periapical radiographs (PRs) have several well-established limitations in detecting

radiographic signs of endodontic disease (Bender & Seltzer 1961, Patel et al. 2015). Firstly,

unintentional geometric distortion can result in PR under or overestimation of the size of root

resorption (Forsberg & Halse (1994 & 1997), Vaz de Souza et al. 2017). Secondly,

anatomical noise can result in PR missing or underestimating the size of ECR (Kamburoğlu

et al. 2011, Bernardes et al. 2012). Thirdly, as PRs are 2-dimensional shadowgraphs they

only confirm the height and width of ECR which is confined to the interproximal aspects of

the tooth, information on the depth, and/or circumferential (labial/buccal) spread of ECR is

minimal, i.e. the third dimension is missing (Patel et al. 2017).

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 The limitations of radiographs can result in misdiagnosis, inadequate assessment and/or

poor management of ECR (Gulabivala & Searson 1995, Patel et al. 2009b, Schwartz et al.
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2010, Gunst et al. 2013). The limitations of PR may be overcome with cone beam computed

tomography (Figures 10,12,13).

CBCT overcomes the limitations of PR, allowing ECR to be viewed in any plane without

superimposition of overlying structures and geometric distortion (anatomical noise); in

addition, the reconstructed CBCT images are also more accurate than PR (Hashem et al.

2013, Patel et al. 2015). The radiation dose of a CBCT scan is in the same order of

magnitude as PRs (Loubele et al. 2009, Pauwels et al. 2012, Harvey & Patel 2016). It is now

well established that CBCT can improve the diagnosis and/or management of complex

endodontic problems (Brady et al. 2014, Hashem et al. 2015, Rodríguez et al. 2017, Patel &

Vincer 2017).

The importance of CBCT in the management of ECR is also highlighted in the European

Society of Endodontology [ESE] position statement (2014), and the joint statement by the

American Association of Endodontists & American Academy of Oral & Maxillofacial

Radiology [AAE/AAOMR] (2015).

CBCT has had a major impact on the diagnosis and management of root resorption lesions.

The true nature and extent, i.e. the exact dimensions, degree of circumferential spread and

proximity to the root canal may be appreciated; the fine resorptive extensions of the main

resorptive lesion as well as hard tissue deposits may be clearly visualised (Mavridou et al.

2016b, Patel et al. 2017). This is clinically relevant as these resorptive extensions may

extend apically and/or contain active resorptive tissue allowing ECR to continue to progress

if not diagnosed and appropriately managed. It is possible that the inability to identify and

remove the reparative resorptive tissue may also have a negative impact on the outcome of

treatment (Estevez et al. 2010).

The literature is replete with case (series) reports confirming that PRs do not consistently

reveal the true nature of ECR compared to CBCT (Patel et al. 2007, 2016a, Schwartz et al.

2010, Estevez et al. 2010, Gunst et al. 2013, Salzano & Tirone 2015, Wu et al. 2016). A

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 clinical study compared PR and CBCT for the detection and management of internal and

external cervical resorption lesions (Patel et al. 2009b). Receiver Operator Characteristic
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(ROC) curves as well as the reproducibility of each technique was determined for diagnostic

accuracy and treatment option chosen. The ROC value for PR and CBCT was 0.83 and 1

respectively. This study not only confirmed the superior accuracy of CBCT over PR, but also

that the correct treatment plan was more likely to be chosen when the clinician had access

to CBCT. Similar conclusions have been found in more recent in-vivo studies (Ee et al.

2014, Patel et al. 2016b, Rodriguez et al. 2017a,b).

Using PRs, Heithersay (1999b) devised a PR classification to categorise ECR according to

its extension into the root and proximity to the root canal. In summary, class I, a small

cervical lesion with shallow penetration into dentine; class II, a well-defined lesion close to

the coronal pulp but with little or no extension into radicular dentine; class III, deeper

invasion of the lesion into the coronal third of the root; class IV, a lesion extending beyond

the coronal third of the root (Heithersay 1999b). The limitation of this classification is that it is

only relevant if ECR is solely limited to the proximal aspect of a tooth; this is impossible to

confirm from a 2-dimensional radiograph. Heithersay’s classification does not describe the

true nature of ECR (resorptive and reparative) as it does not describe the third dimension,

i.e. bucco-lingual and/or circumferential spread of ECR, nor does it describe the proximity of

ECR to the root canal.

In an ex vivo study Vaz de Souza et al. (2017) compared the diagnostic efficacy of 2 CBCT

scanners with PR for the detection and classification of simulated external cervical

resorption (ECR) lesions. Simulated ECR lesions representing the 4 Heithersay classes

were created. Examiners were asked to classify and identify the root surface(s) that ECR

extended to with PR and CBCT. The ECR lesions were correctly identified according to the

tooth surface in 87.8% Kodak CBCT, 89.1% Morita CBCT and 49.4% PR cases. The ECR

lesions were correctly classified according to Heithersay classification in 71.4% Kodak

CBCT, 70% Morita CBCT and 32% PR of cases.

This article is protected by copyright. All rights reserved.

 In a clinical study, Patel et al. (2016b) compared the ability of PA and CBCT to detect,

determine the nature and plan the management of ECR. The ROC analysis revealed that
Accepted Article
PR had a limited accuracy to detect the size (0.75), circumferential spread (0.60) and

location of ECR lesions compared to CBCT. This resulted in the PA treatment plan chosen

to manage ECR varying significantly compared to CBCT.

Patel et al. (2017) suggested a 3-dimensional classification for ECR based on the

radiographic findings of PR and CBCT (Table 2). This classification considers the height of a

lesion, it’s circumferential spread and proximity to the root canal. The aim of the

classification is to ensure accurate diagnosis and communication of ECR between clinicians.

In the future, it should allow an objective outcome assessment of the treatment carried out.

The score for the height of the lesion is recorded as ‘1’ for supracrestal defects, ‘2’ for

subcrestal defects, ‘3’ for defects extending into the middle third of the roots and ‘4’ for those

invading the apical third of the roots. The circumferential spread of ECR is recorded as ‘A’

for lesions extending < 90°, ‘B’ for lesions extending >90°to<180°, ‘C’ for lesions extending

>180°to<270°, and ‘D’ for those extending >270°. Finally, the proximity to the root canal is

noted; ECR is confined to dentine is graded as ‘d’, and ‘p’ when there is (probeable) pulpal

involvement.

As with any X-ray image, CBCT scans must be justified and the principles of As Low As

Reasonably Achievable (ALARA) followed (Pauwels et al. 2012, European Society of

Endodontology 2014).

Concluding remarks

 Several potential predisposing factors have been identified for ECR; certain

combinations of these factors result in a higher frequency of ECR. More research is

required to confirm the cause and effect relationship of these potential predisposing

factors.

 The most commonly affected teeth appear to be maxillary incisor, canine, first molar

and mandibular first molar teeth.

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  There are 3 stages in the process of ECR; initiation, progression/resorption and

reparative phase. Resorption and repair/remodelling can progress in parallel at

Accepted Article
different areas of the affected tooth.

 Periapical radiography has significant limitations in the detection, assessment and

treatment planning of ECR. The increased accuracy of CBCT results in not only more

accurate detection and assessment of ECR, but also selection of the most

appropriate treatment plan.

Conflict of Interest statement

The authors have stated explicitly that there are no conflicts of interest in connection with

this article.

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Figure Legends

Figure 1 Comparison of percentage of appearance of potential predisposing factors, as

reported in the work of Heithersay 1999a and Mavridou et al. 2017a

Figure 2 Histological image of the portal of entry, of tooth 26 with ECR showing the

epithelial tissue ingrowth. Resorption is observed simultaneously at enamel and dentin.

Histological staining was performed with a combination of Stevenel’s blue and Von Gieson’s

picrofuchsin, visualizing mineralized tissue (red) and non-mineralized tissue (blue-green).

Figure 3 Histological image of tooth 46 with ECR showing a small portal of entry and

ingrowth of bonelike tissue. Active blastic cells are also found in the reparative bone like

tissue. Histological staining was performed with a combination of Stevenel’s blue and Von

Gieson’s picrofuchsin, visualizing mineralized tissue (red) and non-mineralized tissue (blue-

green).

Figure 4 Active resorption occurring in both dentin and reparative bone like tissue, observed

in tooth 26 with ECR. Resorption of the bonelike tissue is a part of the remodeling process.

Histological staining was performed with a combination of Stevenel’s blue and Von Gieson’s

picrofuchsin, visualizing mineralized tissue (red) and non-mineralized tissue (blue-green).

Figure 5 NanoCT imaging of tooth 13 and 3D modeling using CTan, CTvol and CTvox

softwares, showing the thickness distribution of the pericanalar resorption resistant sheet

(PRRS).

Figure 6: (a)Structure of Pericanalar Resorption Resistant Sheet and pulp tissue. PRRS is

consisted of predentin, dentin and occasionally bonelike tissue. (b) Calcification inside the

pulp. Histological staining was performed with a combination of Stevenel’s blue and Von

This article is protected by copyright. All rights reserved.

 Gieson’s picrofuchsin, visualizing mineralized tissue (red) and non-mineralized tissue (blue-

green).
Accepted Article
Figure 7 (a) Top: (left) Clinical photograph of a symptomatic and discoloured tooth 11,

(middle) Periapical radiograph of tooth 11 which was initially misdiagnosed as subgingival

caries and temporally restored with a provisional restoration. The patient was referred to an

Endodontist who diagnosed ECR which was deemed restorable and subsequently extracted.

(right) Coronal microCT image of the tooth revealing bonelike tissue encompassing the root

canal and extending beyond the mid- third of the root canal. Bottom: NanoCT image of tooth

36 showing Ingrowth of bonelike tissue through the portal of entry. [Supplementary online

only movies (b) Micro CT scan of tooth 21 with ECR, note the reparative nature of the

resorptive lesion in the core of the tooth, as well as the destructive nature on the distal

aspect of the coronal third of the root. (c)Transaxial view of tooth 36 with ECR, note the

reparative nature of the ECR.]

Figure 8 Comparison of percentage of appearance of ECR in different tooth types, as

reported in the work of Heithersay 1999a and Mavridou et al. 2017a.

Figure 9 Periapical radiograph reveals a mesially impacted unerupted 38 with signs of ECR

of unidentifiable aetiology.

Figure 10 A 65-year-old male presented complaining of a pimple on the inner aspect of his

lower jaw, the only potential aetiological factor was previous endodontic treatment under

rubber dam. (A) clinical photograph reveals a 2mm abscess lingual to the 41 (B) periapical

radiograph reveals ECR of the 31 and the 41. (C, D) The sagittal reconstructed CBCT

images reveal that the ECR is reparative in tooth 31 (yellow arrow) and resorptive in tooth 41

(red arrow), and that both teeth are unrestorable. Note the completely different nature of the

ECR in these neighbouring teeth.

Figure 11 A 36 year-old male presented complaining of a pink discolouration on the labial

aspect of tooth 21. (A) clinical photograph confirms the patient’s complaint of a pink

discolouration and also cavitation at the gingival margin, (B, C) parallax periapical

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 radiographs reveals ECR of the 21, note that the canal walls are visible through the

resorptive lesions.
Accepted Article
Figure 12 A 48-year-old male with symptoms of irreversible pulpitis localised to the 16. The

potential aetiological factors were previous dental treatment, including orthodontics and use

of matrix band. (A, B) Buccal and palatal views of the upper right molar region, there are no

obvious clinical or (C) radiographic signs of endodontic or periodontal disease. (D, E, F)

coronal, sagittal and axial reconstructed CBCT scans reveal clear signs of external cervical

resorption (resorptive [red arrow] and reparative [yellow arrow]). The CBCT scan has

resulted in a change of diagnosis and management, this tooth was extracted as the ECR

defect was clearly unrestorable. This lesion cannot be classified with Heithersay

classification as it cannot be visualised of the periapical radiograph. However, it can be

classified as ‘2Cp’ using 3D Patel classification.

Figure 13 A 64-year-old female with no symptoms presented for a routine check up. (A)

clinical examination reveals a pink band of discolouration (green arrow) and a portal of entry

lingually (purple arrow). (B, C) periapical radiographs reveal extensive ECR, note that the

canal is visible through the radiolucency, confirming ECR. (D) coronal, (E) sagittal and (F, G)

axial reconstructed CBCT slices reveal that the ECR-affected tooth is unrestorable. Note the

apical extension of the resorptive lesion. We can classify this lesion as a Heithersay class 3.

However, the circumferential spread, depth and proximity to the pulp cannot be determined

on the periapical radiographs. A 3D classification of ‘3Bp’ Patel classification precisely

describes the lesion and facilitates reporting and communication between clinicians.

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 Type of study Number Comments

Case report/series 112 Aetiology, diagnosis and/or treatment

Accepted Article
Basic research (Biological and 15 Ex vivo radiological, histopathological and
technical laboratory studies) microbiological studies (including animal
studies)

Clinical research 7 Observational and interventional studies

Review article 13 Narrative descriptive papers

Table 1. Publications on ECR, including type of study

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Accepted Article

Figure 1: Comparison of percentage of appearance of potential predisposing factors, as reported in

the work of Heithersay 1999a and Mavridou et al. 2017a

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 Epithelial
tissue
Accepted Article

Dentin
Clastic cells

Clastic cells
Enamel

Figure 2: Histological image of the portal of entry, of tooth 26 with ECR showing the epithelial tissue
ingrowth. Resorption is observed simultaneously at enamel and dentin. Histological staining was
performed with a combination of Stevenel’s blue and Von Gieson’s picrofuchsin, visualizing
mineralized tissue (red) and non-mineralized tissue (blue-green).

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 Area 1
Accepted Article
Calculus

Bonelike tissue

PRRS

Portal of entry

Area 1

Blastic cells

Bonelike
tissue

Figure 3: Histological image of tooth 46 with ECR showing a small portal of entry and ingrowth of
bonelike tissue. Active blastic cells are also found in the reparative bone like tissue. Histological
staining was performed with a combination of Stevenel’s blue and Von Gieson’s picrofuchsin,
visualizing mineralized tissue (red) and non-mineralized tissue (blue-green).

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 Resorption lacunae
on dentin
Dentin
Accepted Article

Reparative
Clastic cells bonelike tissue

Figure 4: Active resorption occurring in both dentin and reparative bone like tissue, observed in
tooth 26 with ECR. Resorption of the bonelike tissue is a part of the remodeling process. Histological
staining was performed with a combination of Stevenel’s blue and Von Gieson’s picrofuchsin,
visualizing mineralized tissue (red) and non-mineralized tissue (blue-green).

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 PRRS
Accepted Article

Figure 5: NanoCT imaging of tooth 13 and 3D modeling using CTan, CTvol and CTvox softwares,
showing the thickness distribution of the pericanalar resorption resistant sheet (PRRS).

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Accepted Article

Bonelike tissue a

Dentin Intact
odontoblastic layer PRRS

Athrophic Predentin
odontoblastic layer
Bonelike
tissue

b PRRS

Pulp stones

Figure 6: (a)Structure of Pericanalar Resorption Resistant Sheet and pulp tissue. PRRS is consisted of
predentin, dentin and occasionally bonelike tissue. (b) Calcification inside the pulp. Histological
staining was performed with a combination of Stevenel’s blue and Von Gieson’s picrofuchsin,
visualizing mineralized tissue (red) and non-mineralized tissue (blue-green).

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Accepted Article

Figure 7: Top: (left) Clinical photograph of a symptomatic and discoloured tooth 11, (middle)
Periapical radiograph of tooth 11 which was initially misdiagnosed as subgingival caries and
temporally restored with a provisional restoration. The patient was referred to an Endodontist who
diagnosed ECR which was deemed restorable and subsequently extracted. (right) Coronal microCT
image of the tooth revealing bonelike tissue encompassing the root canal and extending beyond the
mid- third of the root canal.

Bottom: NanoCT image of tooth 36 showing Ingrowth of bonelike tissue through the portal of entry.

This article is protected by copyright. All rights reserved.

Accepted Article

Figure 8: Comparison of percentage of appearance of ECR in different tooth types, as reported in the
work of Heithersay 1999a and Mavridou et al. 2017a.

This article is protected by copyright. All rights reserved.

Accepted Article

Figure 9. Periapical radiograph reveals a mesially impacted unerupted 38 with signs of ECR
of unidentifiable aetiology.

Figure 10. A 65-year-old male presented complaining of a pimple on the inner aspect of his lower
jaw, the only potential aetiological factor was previous endodontic treatment under rubber dam. (A)
clinical photograph reveals a 2mm abscess lingual to the 41 (B) periapical radiograph reveals ECR of
the 31 and the 41. (C, D) The sagittal reconstructed CBCT images reveal that the ECR is reparative in
tooth 31 (yellow arrow) and resorptive in tooth 41 (red arrow), and that both teeth are
unrestorable. Note the completely different nature of the ECR in these neighbouring teeth.

This article is protected by copyright. All rights reserved.

Accepted Article

Figure 11. A 36 year-old male presented complaining of a pink discolouration on the labial aspect of
tooth 21. (A) clinical photograph confirms the patient’s complaint of a pink discolouration and also
cavitation at the gingival margin, (B, C) parallax periapical radiographs reveals ECR of the 21, note
that the canal walls are visible through the resorptive lesions.

This article is protected by copyright. All rights reserved.

Accepted Article

Figure 12. A 48-year-old male with symptoms of irreversible pulpitis localised to the 16. The
potential aetiological factors were previous dental treatment, including orthodontics and use of
matrix band. (A, B) Buccal and palatal views of the upper right molar region, there are no obvious
clinical or (C) radiographic signs of endodontic or periodontal disease. (D, E, F) coronal, sagittal and
axial reconstructed CBCT scans reveal clear signs of external cervical resorption (resorptive [red
arrow] and reparative [yellow arrow]). The CBCT scan has resulted in a change of diagnosis and
management, this tooth was extracted as the ECR defect was clearly unrestorable. This lesion cannot
be classified with Heithersay classification as it cannot be visualised of the periapical radiograph.
However, it can be classified as ‘2Cp’ using 3D Patel classification.

This article is protected by copyright. All rights reserved.

Accepted Article

Figure 13. A 64-year-old female with no symptoms presented for a routine check up. (A) clinical
examination reveals a pink band of discolouration (green arrow) and a portal of entry lingually
(purple arrow). (B, C) periapical radiographs reveal extensive ECR, note that the canal is visible
through the radiolucency, confirming ECR. (D) coronal, (E) sagittal and (F, G) axial reconstructed
CBCT slices reveal that the ECR-affected tooth is unrestorable. Note the apical extension of the
resorptive lesion. We can classify this lesion as a Heithersay class 3. However, the circumferential
spread, depth and proximity to the pulp cannot be determined on the periapical radiographs. A 3D
classification of ‘3Bp’ Patel classification precisely describes the lesion and facilitates reporting and
communication between clinicians.

This article is protected by copyright. All rights reserved.