External cervical resorption‐part 1: histopathology, distribution … · 2020. 1. 30. · with...

REVIEW

External cervical resorption-part 1: histopathology,distribution and presentation

S. Patel1,2 , A. M. Mavridou3, P. Lambrechts3 & N. Saberi1

1Department of Endodontology, King’s College London Dental Institute, London; 2Specialist Practice, London, UK; and3Department of Oral Health Services, University of Leuven, Leuven, Belgium

Abstract

Patel S, Mavridou AM, Lambrechts P, Saberi N.

External cervical resorption-part 1: histopathology, distribution

and presentation. International Endodontic Journal, 51, 1205–

1223, 2018.

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 dec-

ades, ECR has attracted increased interest; this is in

part due to novel micro-CT and histopathological

techniques for its assessment and also improved radio-

graphic detection using CBCT. This literature review

will cover the aetiology, potential predisposing factors,

histopathology and diagnosis of ECR. Part 2 will

cover the management of ECR.

Keywords: cone beam computed tomography,

external cervical resorption, histology, nano-CT.

Received 9 March 2018; accepted 22 April 2018

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 resorp-

tion is desirable in primary teeth (physiological root

resorption) as it facilitates their exfoliation, and subse-

quent 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 loca-

tion on the root surface as external or internal resorption.

External root resorption may be further subclassified

into surface resorption, external inflammatory resorp-

tion, external cervical resorption, external replacement

resorption and transient apical resorption (Patel & Pitt

Ford 2007, Patel & Saberi 2018). External cervical

resorption (ECR) usually manifests in the cervical aspect

of teeth; it develops as a result of damage to, and/or defi-

ciency of the periodontal ligament (PDL) (Andreasen &

Andreasen 2007) and the subepithelial cementum.

External cervical resorption (ECR) is a dynamic pro-

cess 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 (Th€onen 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 resorp-

tion’, ‘peripheral cervical resorption’, ‘extracanal invasive

resorption’, ‘odontoclastoma’, ‘peripheral inflammatory

Correspondence: Shanon Patel, Department of Endodontol-

ogy, King’s College Dental Institute, Floor 25 – Tower Wing,

Guy’s Hospital, London SE1 9RT, UK (e-mail: shanonpatel@

gmail.com).

International Endodontic Journal, 51, 1205–1223, 2018© 2018 International Endodontic Journal. Published by John Wiley & Sons Ltd

doi:10.1111/iej.12942

1205

http://orcid.org/0000-0003-0614-6951

http://orcid.org/0000-0003-0614-6951

http://orcid.org/0000-0003-0614-6951

https://orcid.org/0000-0001-5343-4353

https://orcid.org/0000-0001-5343-4353

https://orcid.org/0000-0001-5343-4353

root resorption’, ‘supraosseous extracanal invasive resorp-

tion’, ‘idiopathic external resorption’ and ‘ECR’. In addi-

tion to database searches, the ‘early view’ and

prepublication online 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 ref-

erence 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.

Whilst 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 evi-

dence is a combination and amalgamation of clini-

cally 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 treat-

ment-focused nature of many of the previous publica-

tions, 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 misdi-

agnosis (and potential under-reporting) and misman-

agement of ECR.

This review would ideally take the form of a sys-

tematic review of randomized controlled trials. How-

ever, this is not possible as majority of literature on

this topic, as explained and demonstrated above, con-

sists of case (series) reports, review papers and ex vivo

studies, thus, making such a review impossible to per-

form. 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.

Aetiology

Although several potential aetiological factors have

been associated with the development and progression

of the ECR, the aetiology and pathogenesis of ECR are

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 (Fig. 1). These

included extraction of a neighbouring tooth (Gunst

et al. 2013), malocclusion (Vossoughi & Takei 2007),

playing wind instruments (Gunst et al. 2011), peri-

odontitis (Beertsen et al. 2001), autotransplantation

(Kandalgaonkar et al. 2013), transmission of feline

viruses to humans (Von Arx et al. 2009), herpes zos-

ter (Solomon et al. 1986, Ramchandani & Mellor

2007, Patel et al. 2016a), systemic and genetic fac-

tors (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, sponta-

neous resorption of impacted teeth), cysts, tumours

(Fuss et al. 2003) and pressure of erupting canines

applied to lateral incisors (Ericson et al. 2002, Alqer-

ban et al. 2009, Hadler-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 inci-

dence may be partly attributed to increased aware-

ness of ECR (Chen et al. 2010), and increased uptake

of orthodontic 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 prod-

ucts being used nowadays compared to concentra-

tions of 30% H2O2 used in the past (Friedman et al.

1988, Rotstein et al. 1991, Attin et al. 2003). How-

ever, even with this reduced concentration of bleach-

ing agents, diffusion of hydroxyl radicals can damage

Table 1 Publications on ECR, including type of study

Type of study Number Comments

Case report/series 112 Aetiology, diagnosis and/or

treatment

Basic research

(Biological and

technical laboratory

studies)

15 Ex vivo radiological,

histopathological and

microbiological studies

(including animal studies)

Clinical research 7 Observational and

interventional studies

Review article 13 Narrative descriptive papers

External cervical resorption-part 1 Patel et al.

© 2018 International Endodontic Journal. Published by John Wiley & Sons LtdInternational Endodontic Journal, 51, 1205–1223, 20181206

the PDL fibroblasts (Rotstein et al. 1993, Chapple &

Matthews 2007, Lou et al. 2016). Therefore, it is

essential to advise patients of 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).

Mavridou et al. (2017a) reported only a 1.2% asso-

ciation 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 esorption (TR). The prevalence has been

reported to vary significantly from 14.3% to 85%,

depending on the examined cat populations and

the different experimental methodology used (Pet-

tersson 2010). Von Arx et al. (2009) first sug-

gested 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 avul-

sion 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 bacte-

ria-induced inflammation may be involved in ECR

(Beertsen 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 of

108 teeth), with parafunctional habits (13%) (14 of

108 teeth) or extraction of a neighbouring tooth

(12%) (13 of 108 teeth), have a much higher fre-

quency suggesting a multifactorial aetiology. It should

be mentioned that in previous reports, only 20% of

the ECR cases were identified as multifactorial (Hei-

thersay 1999b). This difference is believed to be due to

the establishment of a more systematic experimental

Figure 1 Comparison of percentage of appearance of potential predisposing factors, as reported in the work of Heithersay

1999a and Mavridou et al. 2017a.

Patel et al. External cervical resorption-part 1

International Endodontic Journal, 51, 1205–1223, 2018© 2018 International Endodontic Journal. Published by John Wiley & Sons Ltd 1207

approach (Mavridou et al. 2016b) and to the consider-

ation of an updated list of potential predisposing fac-

tors (Mavridou et al. 2017a).

Histological and 3D characteristics of

ECR

External cervical resorption (ECR) cases share several

common features (Heithersay 1999a, Luso & Luder

2012, Mavridou et al. 2016a). These are (i) the initia-

tion point (portal(s) of entry), (ii) the resorption area

with its channels and external interconnections (por-

tals of exit), (iii) the pericanalar resorption-resistant

sheet (PRRS), (iv) the repair by substitution of the

resorbed tissues by reparative bone-like tissue and

finally, (v) the remodelling of this reparative tissue

(Mavridou et al. 2016a). In root filled teeth, there is

no PRRS area due to its removal during the mechani-

cal preparation of the root canal (Mavridou et al.

2017b).

Portal(s) of entry

Are located in the cementum below the gingival

epithelial attachment. This area has typically two his-

tological patterns (Mavridou et al. 2016a). Firstly, a

connective tissue with a dense inflammatory lympho-

plasmacytic infiltrate, epithelial tissue is often seen to

cover the granulation tissue (Fig. 2) (Lin et al. 2013,

Mavridou et al. 2016a). Secondly, an ingrowth of

reparative bone-like tissue occurs, whilst local fusion

of the adjacent alveolar bone with resorbed dentine

and even resorbed enamel occurs. In any case, the

localized destruction and/or removal of PDL at the

portal of entry are needed for ECR to occur (Karring

et al. 1980, Nyman et al. 1980, Mavridou et al.

2016a) (Fig. 3).

Resorption area containing channels and external

interconnections

Resorptive lesions expand in all three dimensions

away from portal(s) of entry encircling and/or pro-

gressing towards the root canal system, resulting in

the destruction of dental hard tissues (i.e. cementum,

dentine and enamel). Several resorption 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 Peri-

canalar 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 9 30 lm (Mavridou et al. 2016a)

(Fig. 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).

Pericanalar resorption-resistant sheet (PRRS)

Is a nonuniform layer/area with a thickness of 70 up

to 490 lm depending on its location within the root

(Mavridou et al. 2016a) (Fig. 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) (Fig. 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

(Fig. 6a). In other areas of the pulp, the odontoblastic

layer appears intact (Fig. 6a). Histological findings

also include the formation of pulp stones and diffuse

calcifications (Fig. 6b). Other observations included

hyalinosis (thickening of the walls) of the blood ves-

sels and an increase of the deposition of predentine

(Mavridou et al. 2016a).

Clastic cells

Clastic cells

Enamel

Dentine

Epithelial tissue

Figure 2 Histological image of the portal of entry, of tooth

26 with ECR showing the epithelial tissue ingrowth. Resorp-

tion is observed simultaneously at enamel and dentine. His-

tological staining was performed with a combination of

Stevenel’s blue and Von Gieson’s picrofuchsin, visualizing

mineralized tissue (red) and nonmineralized tissue (blue-

green).



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 (Fig. 7a,

b). The reparative tissue appears as a lamellar trabec-

ular bone, with islands of woven bone formed in

regions of rapid bone repair-remodelling cycle. Histo-

logical findings show bone-like related cells (os-

teoblast-like cells, osteocytes) and osteoid tissue

(Mavridou et al. 2016a) (Fig. 3).

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 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) (Fig. 6).

Pathogenesis

External cervical resorption is a dynamic and evolving

process, with destructive and reparative phases (Luso

& Luder 2012, Mavridou et al. 2016a). The patho-

genesis of ECR consists of three main stages:

Resorption initiation

This is the first stage of ECR and is characterized by a

localized destruction/disruption of the normal PDL

structure, including the unmineralized cementum

Portal of entry

PRRS

Bone-like tissue

Calculus

Blastic cells

Bone-liketissue

Area 1

Area 1

Figure 3 Histological image of tooth 46 with ECR showing a small portal of entry and ingrowth of bone-like tissue. Active

blastic cells are also found in the reparative bone-like tissue. Histological staining was performed with a combination of Steve-

nel’s blue and Von Gieson’s picrofuchsin, visualizing mineralized tissue (red) and nonmineralized tissue (blue-green).



leading to the formation of a blood clot and a local-

ized inflammatory response of the exposed dentine

(Polimeni et al. 2006). Macrophages then migrate to

the affected area and, in addition to wound debride-

ment, will result in the formation of granulation tis-

sue (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 (Schroeder &

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 repopu-

late 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, cemen-

tum 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 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,

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 peri-

odontal ligament fibroblasts (Zhang et al. 2013). The

synergetic effect of hypoxia and bacteria in the PDL

may also accelerate the inflammation (G€olz et al.

2015).

Clastic cellsReparative

bone-like tissue

Dentine

Resorption lacunae on dentine

Figure 4 Active resorption occurring in both dentine and

reparative bone-like tissue, observed in tooth 26 with ECR.

Resorption of the bone-like tissue is a part of the remodelling

process. Histological staining was performed with a combina-

tion of Stevenel’s blue and Von Gieson’s picrofuchsin, visual-

izing mineralized tissue (red) and nonmineralized tissue

(blue-green).

PRRS

Figure 5 Nano-CT imaging of tooth 13 and 3D modelling using CTan, CTvol and CTvox softwares, showing the thickness dis-

tribution of the pericanalar resorption-resistant sheet (PRRS).



Resorption progression

Several factors have been suggested as stimulating

factors for ECR to progress. These include infection

(bacteria) (G€olz 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. 2003a,b) caused by chewing, parafunction or a

combination. All these factors may induce a hypoxic

microenvironment, which activates osteoclastogenesis

(Arnett et al. 2003a,b, Knowles & Athanasou 2009,

Arnett 2010) and subsequently helps in the pro-

gression of ECR (Mavridou et al. 2017a). Hypoxia as

a driving force of angiogenesis could influence the

continuous development of highly vascularized

Bone-like tissue

Bone-liketissue

Athrophic odontoblastic layer

Intact odontoblastic layer

Pulp stones

(a)

(b)

DentinePRRS

PRRS

Figure 6 (a) Structure of pericanalar resorption-resistant sheet and pulp tissue. PRRS is consisted of predentine, dentine and

occasionally bone-like tissue. (b) Calcification inside the pulp. Histological staining was performed with a combination of Steve-

nel’s blue and Von Gieson’s picrofuchsin, visualizing mineralized tissue (red) and nonmineralized tissue (blue-green).



(b)(a)

(d) (e)

(c)

Figure 7 (a) Clinical photograph of a symptomatic and discoloured tooth 11, (b) 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 unrestorable and subsequently extracted. (c) Coronal micro-CT image

of the tooth revealing bone-like tissue encompassing the root canal and extending beyond the mid-third of the root canal. Bot-

tom: Nano-CT image of tooth 36 showing ingrowth of bone-like tissue through the portal of entry. [Supplementary online only

Movies S1 and S2 (d) Micro-CT scan of tooth 36 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. (e) Transaxial view of tooth 36

with ECR, note the reparative nature of the ECR.]



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 longi-

tudinally) within the dentine. The direction that clas-

tic cells move in is dependent on inflammatory

mediators (e.g. growth factors, cytokines, prostaglan-

dins etc.) and hormones (e.g. parathyroid hormone

(PTH), calcitonin, 1,25-dihydroxyvitamin D3 (cal-

citriol) (Manolagas 2002, V€a€an€anen 2005). The pres-

ence 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 resistant to

resorption. However, in advanced cases of ECR, the

root canal may become perforated.

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 nor-

mal alveolar bone structure (Levin 2012). This is

regarded as a form of healing. After formation of the

bone-like tissue, active remodelling can occur asyn-

chronously at many sites. During this stage, repair

and remodelling 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

External cervical resorption 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 (Fig. 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 (Hei-

thersay 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 (Chat-

zopoulos 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 asso-

ciated with the increased uptake of orthodontic treat-

ment (e.g. extraction of the first premolar and

orthodontic movement thereafter).

Mavridou et al. (2017a) detected ECR more fre-

quently in younger age groups than reported by Hei-

thersay (1999b). This may be due to a combination

of factors including increased 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 (Hei-

thersay 1999b, Mavridou et al. 2017a).

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

provided detailed and extensive descriptions of the

potential aetiological factors of ECR. However, it must

be stressed that no definitive cause-and-effect relation-

ship 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 con-

tributory. In 15% of the patient examined in Heither-

say’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 (Heither-

say 1999b, Patel et al. 2016a).

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 (Figs 9–11).The diagnosis of ECR defects can be challenging

(Gulabivala & Searson 1995, Schwartz et al. 2010,

Durack & Patel 2016, Patel et al. 2018). The clinical

presentation of ECR defects is determined by their



location and nature. Whilst 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, 2016a,b,c).

These defects bleed profusely on probing as a result of

their vascularity (Trope 2002, Patel et al. 2009a).

Due to their location, ECR may be mistaken for buc-

cal caries, therefore, it is important to differentiate

these lesions by tactile feedback (probing). 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 tis-

sue is the reason behind its profuse bleeding on prob-

ing. Although pink spots may be easily detected by

the patient and/or clinician, they are more challeng-

ing to detect on posterior teeth, especially when they

are located on the interproximal or lingual/palatal

aspects of the tooth (Fig. 11). It must be stressed that

pink spots are relatively rare. Teeth with ECR may

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.



also be discoloured due to pulp necrosis; in these

cases, they will show a grey discolouration (Fig. 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, that is 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.

Radiographic presentation

There is no ‘classic’ radiographic appearance of ECR.

Lesions may be symmetrical or asymmetrical; their

margins vary from being well defined and smooth to

(a)(b)

(c) (d)

Figure 10 A 65-year-old man presented complaining of a pimple on the inner aspect of his lower jaw; the only potential aetio-

logical factor was previous root canal treatment under rubber dam. (a) clinical photograph reveals a 2 mm abscess lingual to

tooth 41 (b) periapical radiograph reveals ECR of teeth 31 and 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.

(a)

(b) (c)

Figure 11 A 36-year-old man presented complaining of a pink discolouration on the labial aspect of tooth 21. (a) Clinical pho-

tograph confirms the patient’s complaint of a pink discolouration and also cavitation at the gingival margin, (b,c) parallax peri-

apical radiographs reveal ECR of tooth 21, note that the canal walls are visible through the resorptive lesions.



poor definition or ragged or even with no clear delin-

eation between ECR and healthy root structure (Dur-

ack & Patel 2016).

External cervical resorption in the ‘resorptive’ phase

will be radiolucent in nature, whereas ECR lesions in

the ‘reparative’ phase will be more radiopaque, that is

a mottled or cloudy appearance as a result of the ossi-

fication of the granulomatous resorptive tissue

(Fig. 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 detect-

able. 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. Lingually/palatally 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 centred 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 distor-

tion 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 (Kamburo�glu et al. 2011, Bernardes et al.

2012). Thirdly, as PRs are 2-dimensional shadow-

graphs, 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

(a) (b) (c)

(d)(e) (f)

Figure 12 A 48-year-old man with symptoms of irreversible pulpitis localized to the 16. The potential aetiological factors were

previous dental treatment, including orthodontics and use of matrix bands. (a,b) Buccal and palatal views of the maxillary right

molar region, there are no obvious clinical or (c) radiographic signs of endodontic or periodontal disease. (d, e and f) coronal,

sagittal and axial reconstructed CBCT scans reveal clear signs of external cervical resorption (resorptive [red arrow] and repara-

tive [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 visualized of

the periapical radiograph. However, it can be classified as ‘2Cp’ using the 3D Patel classification. (Patel & Saberi 2018).



circumferential (labial/buccal) spread of ECR is mini-

mal, that is the third dimension is missing (Patel et al.

2018).

The limitations of radiographs can result in misdi-

agnosis, inadequate assessment and/or poor manage-

ment of ECR (Gulabivala & Searson 1995, Patel et al.

2009b, Schwartz et al. 2010, Gunst et al. 2013). The

limitations of PR may be overcome with cone beam

computed tomography (Figs 10, 12, and 13).

CBCT overcomes the limitations of PR, allowing

ECR to be viewed in any plane without superimposi-

tion 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 magni-

tude as PRs (Loubele et al. 2009, Pauwels et al.

2012, Harvey & Patel 2016). It is now well estab-

lished that CBCT can improve the diagnosis and/or

management of complex endodontic problems (Brady

et al. 2014, Hashem et al. 2015, Patel & Vincer

2017, Rodriguez et al. 2017a,b).

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 & Maxillo-

facial Radiology [AAE/AAOMR] (2015).

CBCT has had a major impact on the diagnosis

and management of root resorption lesions. The true

nature and extent, that is the exact dimensions,

degree of circumferential spread and proximity to

the root canal, may be appreciated; the fine resorp-

tive extensions of the main resorptive lesion as well

as hard tissue deposits may be clearly visualized

(Mavridou et al. 2016b, Patel et al. 2018). This is

clinically relevant as these resorptive extensions may

extend apically and/or contain active resorptive tis-

sue allowing ECR to continue to progress if not

diagnosed and appropriately managed. It is possible

(a) (b) (c)

(d)

(e) (f)

(g)

Figure 13 A 64-year-old woman 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 exten-

sive ECR, note that the canal is visible through the radiolucency, confirming ECR. (d) Coronal, (e) sagittal and (f,g) axial recon-

structed CBCT slices reveal that the ECR-affected tooth is unrestorable. Note the apical extension of the resorptive lesion. The

lesion can be classified as a Heithersay class 3. However, the circumferential spread, depth and proximity to the pulp cannot

be determined on the periapical radiographs. A 3D Patel classification of ‘3Bp’ precisely describes the lesion and facilitates

reporting and communication between clinicians.



that the inability to identify and remove the repara-

tive 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, Estevez et al. 2010, Schwartz et al.

2010, Gunst et al. 2013, Salzano & Tirone 2015, Wu

et al. 2016). A 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 (ROC) curves

as well as the reproducibility of each technique were

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 con-

firmed 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 classifi-

cation to categorize 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 radicu-

lar dentine; class III, deeper invasion of the lesion into

the coronal third of the root; class IV, a lesion extend-

ing 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 dimen-

sion, that is buccolingual 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 two CBCT scan-

ners with PR for the detection and classification of

simulated external cervical resorption (ECR) lesions.

Simulated ECR lesions representing the four Heither-

say 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.

In a clinical study, Patel et al. (2016c) compared

the ability of PA and CBCT to detect, determine

the nature and plan the management of ECR. The

ROC analysis revealed that PR had a limited accu-

racy 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 com-

pared to CBCT.

Patel et al. (2018) suggested a 3-dimensional classi-

fication for ECR based on the radiographic findings of

PR and CBCT (Table 2). This classification considers

the height of a lesion, its circumferential spread and

proximity to the root canal. The aim of the classifica-

tion is to ensure accurate diagnosis and communica-

tion of ECR between clinicians. In future, it should

allow an objective assessment of the outcome treat-

ment in relation to the nature and extent of ECR.

Table 2 The 3 dimensional classification for ECR



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 extend-

ing >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 involve-

ment.

As with any X-ray image, CBCT scans must be jus-

tified 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 mandibu-

lar first molar teeth.

• There are three stages in the process of ECR; initi-

ation, progression/resorption and reparative phase.

Resorption and repair/remodelling can progress in

parallel at different areas of the affected tooth.

• Periapical radiography has significant limitations

in the detection, assessment and treatment plan-

ning 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

The authors have stated explicitly that there are no

conflict of interests in connection with this article.

References

AAE & AAOMR (2015) American Association of Endodon-

tists and American Academy of Oral & Maxillofacial Radi-

ology joint position statement: use of cone beam computed

tomography in endodontics update. Journal of Endodontics

41, 1393–6.

Alqerban A, Jacobs R, Lambrechts P, Loozen G, Willems G

(2009) Root resorption of the maxillary lateral incisor

caused by impacted canine: a literature review. Clinical

Oral Investigations 3, 247–55.

Andreasen JO, Andreasen FM (2007) Textbook and color atlas

of traumatic injuries to the teeth, 4th edn. Copenhagen:

Munksgaard, pp 1358–81.

Arnett TR (2010) Acidosis, hypoxia and bone. Archives of

Biochemistry and Biophysics 503, 103–9.

Arnett TR, Gibbons DC, Utting JC et al. (2003a) Hypoxia is a

major stimulator of osteoclast formation and bone resorp-

tion. Journal of Cellular Physiology 196, 2–8.

Arnett TR, Massey H, Utting JC, Orriss IR, Flanagan AM

(2003b) Hypoxia is a major stimulator of osteoclast forma-

tion from human peripheral blood. Calcified Tissue Interna-

tional 72, 345–6.

Arroyo-Bote S, Bucchi C, Manzanares C (2017) External cer-

vical resorption. a new oral manifestation of systemic scle-

rosis. Journal of Endodontics 43, 1740–3.

Attin T, Paque F, Ajam F, Lennon AM (2003) Review of the

current status of tooth whitening with the walking bleach

technique. International Endodontic Journal 36, 313–29.

Bastone EB, Freer TJ, McNamara JR (2000) Epidemiology of

dental trauma: a review of the literature. Australian Dental

Journal 45, 2–9.

Beertsen W, Piscaer M, Van Winkelhoff AJ, Everts V (2001)

Generalized cervical root resorption associated with peri-

odontal disease. Journal of Clinical Periodontology 28,

1067–73.

Belibasakis GN, Bostanci N, Hashim A et al. (2007) Regula-

tion of RANKL and OPG gene expression in human gingi-

val fibroblasts and periodontal ligament cells by

Porphyromonas gingivalis: a putative role of the Arg-gin-

gipains. Microbial Pathogenesis 43, 46–53.

Bender IB, Seltzer S (1961) Roentgenographic and direct

observation of experimental lesions in bone: I. Journal of

the American Dental Association 62, 152–60.

Bergmans L, Van Cleynenbreugel J, Verbeken E, Wevers M,

Van Meerbeek B, Lambrechts P (2002) Cervical external

root resorption in vital teeth, X-ray microfocus-tomogra-

phical and histopathological case study. Journal of Clinical

Periodontology 29, 580–5.

Bernardes RA, de Paulo RS, Pereira LO, Duarte MA, Ordi-

nola-Zapata R, de Azevedo JR (2012) Comparative study

of cone beam computed tomography and intraoral periapi-

cal radiographs in diagnosis of lingual-simulated external

root resorptions. Dental Traumatology 28, 268–72.

Bhuva B, Barnes JJ, Patel S (2011) The use of limited cone

beam computed tomography in the diagnosis and manage-

ment of a case of perforating internal root resorption.

International Endodontic Journal 44, 777–86.

Booij-Vrieling HE (2010) Tooth resorption in cats, contribu-

tion of vitamin D and inflammation. (Ph.D. Thesis)

Utrecht, the Netherlands: Faculty of Veterinary medicine.



Brady E, Mannocci F, Brown J, Wilson J, Wilson R, Patel S

(2014) A comparison of cone beam computed tomography

and periapical radiography for the detection of vertical

root fractures in endodontically treated teeth. International

Endodontic Journal 47, 735–46.

Camps J, de Franceschi H, Idir F, Roland C, About I (2007)

Time-course diffusion of hydrogen peroxide through

human dentin: clinical significance for young tooth inter-

nal bleaching. Journal of Endodontics 33, 455–9.

Chapple IL, Matthews JB (2007) The role of reactive oxygen

and antioxidant species in periodontal tissue destruction.

Periodontology 2000 43, 160–232.

Chatzopoulos GS, Sanchez M, Cisneros A, Wolff LF (2017)

Prevalence of temporomandibular symptoms and para-

functional habits in a university dental clinic and associa-

tion with gender, age, and missing teeth. The Journal of

Craniomandibular & Sleep Practice 16, 1–9.

Chen SS, Greenlee GM, Kim JE, Smith CL, Huang GJ (2010)

Systematic review of self-ligating brackets. American Jour-

nal of Orthodontics and Dentofacial Orthopedics 137,

726e721–726 e718.

Durack C, Patel S (2016) Root resorption. In: Patel S, Har-

vey S, Shemesh H, Durack C, eds. Cone Beam Computed

Tomography In Endodontics, 1st edn. Berlin, Germany:

Quintessence Publishing Co. Ltd, pp. 119–31.

Durack C, Patel S, Davies J, Wilson R, Mannocci F (2011)

Diagnostic accuracy of small volume cone beam computed

tomography and intraoral periapical radiography for the

detection of simulated external inflammatory root resorp-

tion. International Endodontic Journal 44, 136–47.

Edwards PC, McVaney T (2005) External cervical root resorp-

tion involving multiple maxillary teeth in a patient with

hereditary hemorrhagic telangiectasia. Oral Surgery, Oral

Medicine, Oral Pathology, and Oral Radiology 5, 585–91.

Ee J, Fayad MI, Johnson BR (2014) Comparison of endodon-

tic diagnosis and treatment planning decisions using cone-

beam volumetric tomography versus periapical radiogra-

phy. Journal of Endodontics 40, 910–6.

Ericson S, Bjerklin K, Falahat B (2002) Does the canine den-

tal follicle cause resorption of permanent incisor roots? A

computed tomographic study of erupting maxillary cani-

nes. Angle Orthodontist 2, 95–104.

Estevez R, Aranguren J, Escorial A et al. (2010) Invasive cer-

vical resorption Class III in a maxillary central incisor:

diagnosis and follow-up by means of cone-beam computed

tomography. Journal of Endodontics 36, 2012–4.

European Society of Endodontology (2014) European soci-

ety of endodontology position statement: the use of

CBCT in endodontics. International Endodontic Journals

47, 502–4.

Forsberg J, Halse A (1994) Radiographic simulation of a

periapical lesion comparing the paralleling and the bisect-

ing-angle techniques. International Endodontic Journal 27,

133–8.

Forsberg J, Halse A (1997) Periapical radiolucencies as eval-

uated by bisecting-angle and paralleling radiographic tech-

niques. International Endodontic Journal 30, 115–23.

Frank AL, Torabinejad M (1998) Diagnosis and treatment of

extracanal invasive resorption. Journal of Endodontics 24,

500–4.

Friedman S, Rotstein I, Libfield H, Stabholz A, Heling I

(1988) Incidence of external root resorption and esthetic

results in 58 bleached pulpless teeth. Endodontics & Dental

Traumatology 4, 23–6.

Fukushima H, Kajiya H, Takada K, Okamoto F, Okabe K (2003)

Expression and role of RANKL in periodontal ligament cells

during physiological root-resorption in human deciduous

teeth. European Journal of Oral Sciences 111, 346–52.

Fuss Z, Tsesis I, Lin S (2003) Root resorption-diagnosis, clas-

sification and treatment choices based on stimulation fac-

tors. Dental Traumatology 4, 175–82.

G€olz L, Memmert S, Rath-Deschner B et al. (2015) Hypoxia

and P. gingivalis synergistically induce HIF-1 and NF-jB

activation in PDL cells and periodontal diseases. Mediators

of Inflammation 2015, 438085.

Gulabivala K, Searson LJ (1995) Clinical diagnosis of inter-

nal resorption: an exception to the rule. International


Gunst V, Huybrechts B, De Almeida Neves A, Bergmans L,

Van Meerbeek B, Lambrechts P (2011) Playing wind

instruments as a potential aetiologic cofactor in external

cervical resorption: two case reports. International Endodon-

tic Journal 44, 268–82.

Gunst V, Mavridou A, Huybrechts B, Van Gorp G, Bergmans

L, Lambrechts P (2013) External cervical resorption: an

analysis using cone beam and microfocus computed

tomography and scanning electron microscopy. Interna-

tional Endodontic Journal 46, 877–87.

Hadler-Olsen S, Pirttiniemi P, Kerosuo H et al. (2015) Root

resorptions related to ectopic and normal eruption of max-

illary canine teeth - A 3D study. Acta Odontologica Scandi-

navica 8, 609–15.

Harvey S, Patel S (2016) Using CBCT: dose, risks and arte-

facts. In: Patel S, Harvey S, Shemesh H, Durack C, eds.

Cone Beam Computed Tomography In Endodontics, 1st edn.

Berlin, Germany: Quintessence Publishing Co., Ltd., pp

43–53.

Hashem D, Brown JE, Patel S et al. (2013) An in vitro com-

parison of the accuracy of measurements obtained from

high- and low-resolution cone-beam computed tomogra-

phy scans. Journal of Endodontics 39, 394–7.

Hashem D, Mannocci F, Patel S et al. (2015) Clinical and

radiographic assessment of the efficacy of calcium silicate

indirect pulp capping a randomized controlled clinical

trial. Journal of Dental Research 94, 562–8.

Heithersay GS (1999a) Clinical, radiologic, and histopatho-

logic features of invasive cervical resorption. Quintessence

International 30, 27–37.



Heithersay GS (1999b) Invasive cervical resorption: an anal-

ysis of potential predisposing factors. Quintessence interna-

tional 30, 83–95.

Heithersay GS (2004) Invasive cervical resorption. Endodontic

Topics 7, 73–92.

Iqbal MK (2007) Clinical and scanning electron microscopic

features of invasive cervical resorption in a maxillary

molar. Oral Surgery, Oral Medicine, Oral Pathology, Oral

Radiology and Endodontology 103, 49–5.

Kamburo�glu K, Kurs�un S, Y€uksel S, Oztas� B (2011) Observer

ability to detect ex vivo simulated internal or external cervi-

cal root resorption. Journal of Endodontics 37, 168–75.

Kandalgaonkar SD, Gharat LA, Tupsakhare SD, Gabhane

MH (2013) Invasive cervical resorption: a review. Journal

of International Oral Health 5, 124–30.

Kanzaki H, Chiba M, Shimizu Y, Mitani H (2001) Dual regu-

lation of osteoclast differentiation by periodontal ligament

cells through RANKL stimulation and OPG inhibition.

Journal of Dental Research 80, 887–91.

Karring T, Nyman S, Linde J (1980) Healing following

implantation of periodontitis affected roots into bone tis-

sue. Journal of Clinical Periodontology 7, 96–105.

Knowles HJ, Athanasou NA (2009) Canonical and non-

canonical pathways of osteoclast formation. Histology and

Histopathology 24, 337–46.

Le LM, Yi J, Yang Y et al. (2016) Compression and hypoxia

play independent roles while having combinative effects in

the osteoclastogenesis induced by periodontal ligament

cells. Angle Orthodontist 86, 66–73.

Levin LG (2012) Tooth resorption. In: Hargreaves KM, Goodis

HE, Tay FR, eds. Seltzer and Benders Dental Pulp, 2nd edn.

Hanover Park, IL, USA: Quintessence Publishing Co, pp

397–419.

Lin HJ, Chan CP, Yang CY et al. (2011) Cemental tear: clini-

cal characteristics and its predisposing factors. Journal of

Endodontics 37, 611–8.

Lin YP, Love RM, Friedlander LT, Shang HF, Pai MH (2013)

Expression of Toll-like receptors 2 and 4 and the OPG–

RANKL–RANK system in inflammatory external root

resorption and external cervical resorption. International


Line SE, Polson AM, Zander HA (1974) Relationship

between periodontal injury, selective cell repopulation and

ankylosis. Journal of Periodontoly 45, 725–30.

Llena-Puy MC, Amengual-Lorenzo J, Forner-Navarro L

(2002) Idiopathic external root resorption associated to

hypercalciuria. Medicina Oral 7, 192–9.

Lou EK, Cathro P, Marino V, Damiani F, Heithersay GS

(2016) Evaluation of hydroxyl radical diffusion and acidi-

fied thiourea as a scavenger during intracoronal bleach-

ing. Journal of Endodontics 7, 1126–30.

Loubele M, Bogaerts R, Van Dijck E et al. (2009) Comparison

between effective radiation dose of CBCT and MSCT scan-

ners for dentomaxillofacial applications. European Journal of

Radiology 71, 461–8.

Luso S, Luder HU (2012) Resorption pattern and radio-

graphic diagnosis of invasive cervical resorption. A correl-

ative micro-CT, scanning electron and light microscopic

evaluation of a case series. Schweizerische Monatsschrift f€ur

Zahnmedizin 122, 914–30.

Manolagas SC (2002) Birth and death of bone cells: basic

regulatory mechanisms and implications for the pathogen-

esis and treatment of osteoporosis. Endocrine Reviews 2,

115–37.

Mavridou AM, Hauben E, Wevers M, Schepers E, Bergmans

L, Lambrechts P (2016a) Understanding external cervical

tooth resorption in vital teeth. Journal of Endodontics 42,

1737–51.

Mavridou AM, Pyka G, Kerckhofs G et al. (2016b) A novel mul-

timodular methodology to investigate external cervical tooth

resorption. International Endodontic Journal 49, 287–300.

Mavridou AM, Bergmans L, Barendregt D, Lambrechts P

(2017a) Descriptive analysis of factors associated with

external cervical resorption. Journal of Endodontics 43,

1602–10.

Mavridou AM, Hauben E, Wevers M, Schepers E, Bergmans

L, Lambrechts P (2017b) Understanding external cervical

tooth resorption patterns in endodontically treated teeth.

International Endodontic Journal 12, 1116–33.

Melcher AH (1970) Repair of wounds in the periodontium of

the rat. Influence of periodontal ligament on osteogenesis.

Archives of Oral Biology 15, 1183–204.

Moskow BS (1989) Periodontal manifestations of hyperox-

alouria and oxalosis. Journal of Periodontology 60, 271–8.

Neely AL, Gordon SC (2007) A familial pattern of multiple

idiopathic cervical root resorption in a father and son: a

22-year follow up. Journal of periodontology 78, 347–71.

Neuvald L, Consolaro A (2000) Cementoenamel junction:

Microscopic analysis and external cervical resorption. Jour-

nal of Endodontics 26, 503–8.

Niklas A, Proff P, Gosau M, R€omer P (2013) The role of

hypoxia in orthodontic tooth movement. International Jour-

nal of Dentistry 2013, 841840.

Nyman S, Karring T, Lindhe J, Plant�en S (1980) Healing fol-

lowing implantation of periodontitis-affected roots into gin-

gival connective tissue. Journal of Clinical Periodontology 7,

394–401.

Nyman S, Houston F, Sarhed G, Lindhe J, Karring T (1985)

Healing following reimplantation of teeth subjected to root

planing and citric acid treatment. Journal of Clinical Peri-

odontology 29, 294–305.

Patel S, Pitt Ford T (2007) Is the resorption external or

internal? Dental Update 34, 218–29.

Patel S, Saberi N (2015) External cervical resorption associ-

ated with the use of bisphosphonates: a case series. Journal

of Endodontics 41, 742–8.

Patel S, Vincer L (2017) Case report: single visit indirect

pulp cap using biodentine. Dental Update 44, 141–5.

Patel S, Dawood A, Ford TP, Whaites E (2007) The potential

applications of cone beam computed tomography in the



management of endodontic problems. International


Patel S, Kanagasingam S, Ford PT (2009a) External cervical

resorption: a review. Journal of Endodontics 35, 616–25.

Patel S, Dawood A, Wilson R, Horner K, Mannocci F

(2009b) The detection and management of root resorption

lesions using intraoral radiography and cone beam com-

puted tomography - an in vivo investigation. International


Patel S, Durack C, Abella F, Shemesh H, Roig M, Lemberg K

(2015) Cone beam computed tomography in endodontics

– a review. International Endodontic Journal 48, 3–15.

Patel S, Durack C, Ricucci D (2016a) Root resorption. In:

Hargreaves KM, Berman LH, eds. Pathways of the pulp,

11th edn. St Louis, USA: Elsevier, pp 660–83.

Patel K, Schirru E, Niazi S, Mitchell P, Mannocci F (2016b)

Multiple apical radiolucencies and external cervical resorp-

tion associated with varicella zoster virus: a case report.

Journal of Endodontics 42, 978–83.

Patel K, Mannocci F, Patel S (2016c) The assessment

and management of external cervical resorption with

periapical radiographs and cone-beam computed

tomography: a clinical study. Journal of Endodontics 42,

1435–40.

Patel S, Foschi F, Mannocci F, Patel K (2018) External cervi-

cal resorption: a three-dimensional classification. Interna-

tional Endodontic Journal 51, 206–14.

Patel S, Saberi N (2018) The ins and outs of root resorption.

British Dental Journal 224, 691–9.

Pauwels R, Beinsbergera J, Collaert B et al. (2012) Effective

dose range for dental cone beam computed tomography

scanners. European Journal of Radiology 81, 267–71.

Pettersson A (2010) Tooth resorption in the Swedish Eura-

sion Lynx (Lynx lynx). Journal of Veterinary Dentistry 27,

222–6.

Polimeni G, Xiropaidis AV, Wikesj€o UM (2006) Biology and

principles of periodontal wound healing/regeneration. Peri-

odontology 2000 41, 30–47.

Proffit WR, Jackson TH, Turvey TA (2013) Changes in the

pattern of patients receiving surgicalorthodontic treat-

ment. American Journal of Orthodontics and Dentofacial

Orthopedics 143, 793–8.

Ramchandani PL, Mellor TK (2007) Herpes zoster associated

with tooth resorption and periapical lesions. British Journal

of Oral and Maxillofacial Surgery 45, 71–3.

RIZIV (2017) National Institute for Health and Disability

Insurance, Belgium (www document) URL http://www.

riziv.fgov.be/nl/statistieken/Paginas/default.aspx#.Wjo

ZAMv6vug (accessed on 7 November 2017).

Rodriguez G, Abella F, Dur�an-Sindreu F, Patel S, Roig M

(2017a) Influence of cone-beam computed tomography in

clinical decision making among specialists. Journal of


Rodriguez G, Patel S, Dur�an-Sindreu F, Roig M, Abella F

(2017b) Influence of cone-beam computed tomography on

endodontic retreatment strategies among general dental

practitioners and endodontists. Journal of Endodontics 43,

1433–7.

Rombouts C, Giraud T, Jeanneau C, About I (2017) Pulp

vascularization during tooth development, regeneration

and therapy. Journal of Dental Research 96, 137–44.

Rotstein I, Torek Y, Misgav R (1991) Effect of cementum

defects on radicular penetration of 30% hydrogen peroxide

during intracoronal bleaching. Journal of Endodontics 17,

230–3.

Rotstein I, Mor C, Friedman S (1993) Prognosis of intra-

coronal bleaching with sodium perborate prepara-

tion in vitro: 1-year study. Journal of Endodontics 19,

10–2.

Sackett DL, Rosenberg WMC, Gray JMA, Haynes RB, Richard-

son WS (1996) Evidence based medicine: what it is and

what it isn’t. British Medical Journal 312, 71–2.

Salzano S, Tirone F (2015) Conservative nonsurgical treat-

ment of class 4 invasive cervical resorption: a case series.

Journal of Endodontics 41, 1907–12.

Schroeder HE, Scherle WF (1988) Cemento-enamel junction-

Revisited. Journal of Periodontal Research 23, 53–9.

Schwartz RS, Robbins JW, Rindler E (2010) Management of

invasive cervical resorption: observations from three pri-

vate practices and a report of three cases. Journal of


Solomon CS, Coffiner MO, Chalfin HE (1986) Herpes zoster

revisited: implicated in root resorption. Journal of Endodon-

tics 12, 210–3.

Th€onen A, Pettom€akt T, Patcas R, Zehnder M (2013) Occur-

rence of cervical invasive root resorption in first and sec-

ond molar teeth of orthodontic patients eight years after

bracket removal. Journal of Endodontics 39, 27–30.

Trope M (2002) Root resorption due to dental trauma.

Endodontic Topics 1, 79–100.

Uchiyama M, Nakamichi Y, Nakamura M et al. (2009) Den-

tal pulp and periodontal ligament cells support osteoclastic

differentiation. Journal of Dental Research 88, 609–14.

V€a€an€anen K (2005) Mechanism of osteoclast mediated bone

resorption-rationale for the design of new therapeutics.

Advanced Drug Delivery Reviews 7, 959–71.

Van der Heyden J (2013) Report 3: Use of Healthwelfare Ser-

vices in Health Interview Survey 2013. Belgium: Scientific

Institute of Public Health (ISP-WIV), Brussels.

Vaz de Souza D, Schirru E, Mannocci F, Foschi F, Patel S

(2017) External cervical resorption: a comparison of the

diagnostic efficacy using 2 different cone-beam computed

tomographic units and periapical radiographs. Journal of


Von Arx T, Schawalder P, Ackermann M, Bosshardt DD

(2009) Human and feline invasive cervical resorptions:

the missing link? Presentation of four cases. Journal of


Vossoughi R, Takei HH (2007) External cervical resorption

associated with traumatic occlusion and pyogenic



http://www.riziv.fgov.be/nl/statistieken/Paginas/default.aspx#.WjoZAMv6vug



granuloma. Journal of the Canadian Dental Association 73,

625–8.

Wedenberg C (1987) Evidence for a dentin-derived inhibitor

of macrophage spreading. Scandinavian Journal of Dental

Research 95, 381–8.

Wu J, Lin LY, Yang J et al. (2016) Multiple idiopathic cervi-

cal root resorption: a case report. International Endodontic

Journal 49, 189–202.

Zhang HY, Liu R, Xing YJ, Xu P, Li Y, Li CJ (2013) Effects of

hypoxia on the proliferation, mineralization and ultra-

structure of human periodontal ligament fibroblasts

in vitro. Experimental and Therapeutic Medicine 6, 1553–9.

Supporting Information

Additional Supporting Information may be found in

the online version of this article:

Movie S1. 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.

Movie S2. Transaxial view of tooth 36 with ECR,

note the reparative nature of the ECR.

International Endodontic Journal, 51, 1205–1223, 2018© 2018 International Endodontic Journal. Published by John Wiley & Sons Ltd


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