apical resorption in teeth with periapical lesions: correlation between radiographic diagnosis and...

ORIGINAL RESEARCH

Apical resorption in teeth with periapical lesions: Correlationbetween radiographic diagnosis and SEM examinationaej_196 2..7

Fabiana Vieira Vier-Pelisser, DDS, PhD1; José Antonio Poli de Figueiredo, DDS, MSc, PhD1;Marcus Vinícius Reis Só, DDS, MSc, PhD2; Lisiane Estivallet, DDS3; and Sílvia Juliana Eickhoff, DDS3

1 Pontifical Catholic University of Rio Grande do Sul – PUCRS, Porto Alegre, Brazil

2 Federal University of Rio Grande do Sul, Porto Alegre, RS, Brazil

3 ULBRA, Canoas, RS, Brazil

Keywordsexternal apical resorption, radiograph

diagnosis, SEM.

CorrespondenceDr Jose Antonio Poli de Figueiredo,

Post-Graduate Program in Dentistry, Pontifical

Catholic University of Rio Grande do Sul –

PUCRS, Av. Ipiranga 6681 Prédio 6 sala 206,

CEP 90619-900 Porto Alegre, RS, Brazil.

Email: [email protected]

doi:10.1111/j.1747-4477.2009.00196.x

Abstract

This study correlated the radiographic findings and scanning electron micros-copy (SEM) images of external apical resorption (EAR) in teeth with periapicallesions. Standard radiographs were taken from 45 teeth with periapical lesionsbefore their extraction. Using a radiographic examination, the root apex ofeach tooth was classified according to the EAR into the following categories:radiographic external apical resorption (REAR) absent, superficial and deep.The apical root surface was also examined with SEM. Photomicrographs ofEARs were classified as periforaminal (PEAR) and foraminal (FEAR) in threedegrees: 0, 1 and 2. REAR was present in 72.5% of cases, of which 20% weredeep. Based upon SEM analysis, PEAR and FEAR occurred in 75.6% and66.7% of cases respectively; 51.2% and 59% respectively, of these teethreceived a score of 2. Only 15.4% of the specimens were unaffected by EAR.

When teeth with periapical lesions were examined for EAR with bothradiography and by SEM, there was no correlation between the findings.

Introduction

Bacterial infection in teeth with pulp necrosis promotesmodifications in the standard structural morphology ofperiapical tissues as well as the establishment of periapicalinflammatory lesions (1).

A periapical lesion with a visible radiolucency is gen-erally accompanied by some degree of root resorption.Several authors (2–5) have verified that root resorption iscommonly present when pathologic tissue surrounds thetooth apex. Henry and Weinmann (6) reported that smallareas of resorption could only be diagnosed with idealradiographs.

Periapical inflammation and medullar bone destructioncan exist without radiographic detection. Apical lesionsare only visible when cortical bone is resorbed (7).Although rarely detected by radiographs, previous studies(8–11) have verified that root resorption constantlyoccurs in association with apical lesions.

The conventional radiograph is two-dimensional andhas limitations for quantitative detection and localisationof external resorptions in teeth with periapical lesions(5,12). Ferlini Filho (12) concluded that root resorptionsdetected by light microscopy (94.44% of cases) wereradiographically observed in only 36.11% of the samples.

Several authors (11,13–15) used scanning electronmicroscopy (SEM) techniques to examine the apicalforamina and surrounding tissue of teeth with chroniclesions. Underlying the granulomatous tissue, the authorsfound normal cement. They also observed eroded andresorbed areas arising because of the inflammation,which may extend to the internal surface of the rootcanal.

Lomçali et al. (16) reported the presence of resorptionlacunae on root external surfaces, which act as nichesfacilitating the deposition and accumulation of periapicalbacterial biofilm. Vier and Figueiredo (17) reported nocorrelation between the diagnosis of periapical lesions

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2 © 2009 The Authors

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and the extension of external apical resorption (EAR) andthey verified that periforaminal and foraminal resorp-tions were present in 87.3% and 83.2% of the apexes,respectively. This resorption extended to the interior ofthe root canal in 74.7% of their cases (18).

The purpose of this study was to correlate the radio-graphic examination and SEM examination of EAR inteeth with radiographically visible periapical lesions.

Materials and methods

This study was approved by the Ethics Committee of theLutheran University of Brazil under the protocol number044/2001.

Forty-five permanent human teeth, extracted for beingunrestorable because of the great extent of coronal tissuedestruction, were examined. All teeth had completelyformed roots and showed radiographically visible periapi-cal lesions, ranging in size from 0.2 to 1.0 cm, and hadhad received no previous endodontic treatment. Teethwith extensive apical lesions that encroached on the rootcervical area were not used in this study to exclude thepossibility of endo-periodontal lesions.

The teeth were collected from public health centres,the School of Dentistry at ULBRA/Canoas, private dentalclinics and corporate health clinics.

Individually labelled plastic vials containing a 10% for-malin solution for storing the specimens were distributedto these locations. Radiographic film (Ektaspeed plus;Eastman Kodak Co., Rochester, NY, USA) was attached tothe plastic vial and labelled with the same number asthe vial.

Before extraction, the teeth were radiographed accord-ing to the routine procedures of each collection location.The X-ray equipment where the samples were obtainedwas from the same commercial brand (Dabi Atlante,Ribeirao Preto, Brazil), operating at 70 KV. Teeth thatfilled the requirements previously described wereincluded in this experiment. A new radiograph was takenbefore tooth extraction using radiographic positioners(Jon Han-Shin, São Paulo, SP, Brazil) in order to obtainstandard vertical and horizontal angulations of theimages. The radiographic equipment available at eachcollection location was used, and the exposure time wasset at 1 s.

After extraction, teeth were placed in vials containing a10% formalin solution and identified.

Radiograpic processing was performed at the UFRGSDepartment of Radiology using an automatic processingmachine (Dental X-Ray Processor, Des Plaines, IL, USA).The developing and fixation time was 4.5 min. The radio-graphs were analysed by three examiners with the aid of

a 15¥ magnifying glass in a negatoscope, and a blackpaper frame surrounded the film to support analysis.

The apical portions of the roots were analysed accord-ing to the criteria for classifying EAR in radiographspreviously described by Ferlini Filho (12): Absent: rootwithout alteration; Superficial: one or more cup-like radi-olucencies not deeper than nearly 1 mm; Deep: identicalto the superficial profile except extending more than1 mm deep. In advanced processes, these features couldbe associated with root shortening.

The apical 3 mm of each root were sectioned withwater-cooled carborundum discs. The root apexes wereplaced in individual plastic vials containing a 2.5%sodium hypochlorite solution (Pharmacy School ofULBRA/Canoas, RS, Brazil) for 3 h.

The specimens were dehydrated in increasing con-centrations of alcohol (70%, 90% and 99%) (PharmacySchool of ULBRA/Canoas, RS, Brazil) for 5 h each, thenplaced on metallic stubs, indentified and metalised with a150 Å thickness of gold palladium (MED 020; BAL-TEC,Balzers, Liechtenstein). SEM was performed at the Elec-tronic Microscopy Laboratory of ULBRA/Canoas – RSusing a Philips XL 20 Scanning Electron Microscope(Philips, Eindhoven, Netherlands), operating at 15 KV.

Roots with more than one main apical foramen werephotographed twice so that all foramina could be analy-sed. The photomicrographs were analysed separately bytwo previously calibrated examiners.

The apexes were classified according to their periforami-nal EAR (PEAR) (area that circumscribes the apicalforamen) and foraminal EAR (FEAR) (area that limits theprofile or apical foramen perimeter) according to modifiedcriteria based on those described by Vier and Figueiredo(17): Level 0: absence of resorption; Level 1: resorptionaffecting up to 1/4 of the examined area; Level 2: resorp-tion affecting more than 1/4 of the examined area.

When teeth had two or more apical foramina or hadfused roots, the level of final resorption represented theforamen in which resorption was most pronounced.Final diagnosis of radiographic external apical resorption(REAR) was the one determined by at least two of thethree observers. When there was no agreement betweentwo observers, as to the diagnosis of REAF or REAP, theywould re-assess the images together to reach a consensus.

Kendall’s coefficient of agreement and Kappa’s coeffi-cient were applied to evaluate the level of agreementbetween the examiners of the radiographic exam andSEM evaluation, respectively.

Kappa’s coefficient was also used to analyse the corre-lation between EAR diagnosed radiographically and bySEM. The correlation was established between the fol-lowing measurements: REAR ¥ PEAR, REAR ¥ FEAR,and REAR ¥ EAR in the final SEM (SEM EAR).

F. V. Vier-Pelisser et al. Apical Resorption in Teeth

3© 2009 The Authors


To establish the SEM EAR level, the most pronouncedresorption level (regardless of whether it was perifora-minal (PEAR) or foraminal (FEAR)) was chosen. Forexample, if PEAR was 2 and FEAR 1, then we noted theSEM EAR as 2.

Results

Our results were divided into three parts and areexpressed in Tables 1–4:

Radiographic evaluation of EAR

The level of agreement among the three examiners(evaluated by Kendall’s coefficient of agreement) was 0.6.Five radiographs from a total of 45 were lost duringprocessing.

Forty dental apexes were radiographically evaluated(Table 1), and 72.5% presented some level of resorption.Of these, 52.5% were classified as superficial (Fig. 1b)and 20.0% as deep (Fig. 1c). Only 27.5% were totallylacking resorption (Fig. 1a).

SEM examination of EAR

The level of agreement among the examiners measuredusing the Kappa’s coefficient was 0.8. Of the 45 specimensanalysed, four were either lost during preparation for SEMor impossible to classify based on resorption level.

Regardless of level of extension, periforaminal resorp-tion was present in 75.6% and foraminal resorption in66.7% of the apexes analysed (Fig. 2b–d, Table 2). Teethin which apical resorption affected more than 1/4 of thearea examined (level 2) were found in 51.2% and 59.0%of the cases with periforaminal and foraminal resorption,respectively.

The absence of resorption (periforaminal or foraminal)was observed in 15.4% of the specimens (Table 3,Fig. 2a). While 84.6% of cases showed some level ofresorption, 35.9% of the cases exhibited resorption affect-ing more than 1/4 of the periforaminal and foraminalareas (Fig. 2b–d).

Correlation between radiographic diagnosis andSEM examination of EAR

It was possible to compile EAR data from 36 of the 40radiographic images and 41 photomicrographs. TheKappa’s coefficient indicated that there was no correla-tion between radiographic diagnosis and SEM examina-tion (Kappa = 0). This was true when both periforaminaland foraminal resorption were analysed independently(REAR ¥ PEAR and REAR ¥ FEAR) as well as when thetwo conditions were associated to examine those teethwhere resorption was most pronounced (REAR ¥ SEMEAR).

In 63.9% of cases (Table 4), SEM examination showeda more significant resorption pattern (Fig. 2b) than thatobserved radiographically (Fig. 1a). Agreement betweenthese methods was found in only 19.5% of teeth. In16.7% of cases, resorption detected radiographically wassuperior to that recorded by SEM.

Discussion

Considering the limitations of a radiographic exam fordiagnosing dental resorption, this study attempted toobserve teeth with radiographically visible periapicallesions. We aimed to correlate the routine findings of thisprocess to the topographical features of the root apex

Table 1 Presence and extension of external apical resorption diagnosed

in periapical radiographs

n %

Absent 11 27.5

Superficial 21 52.5

Deep 8 20.0

Total 40 100.0

Table 2 Extension levels of periforaminal and foraminal external apical

resorptions of dental apexes examined by scanning electron microscopy

Resorption level

Resorption

Periforaminal Foraminal

F % F %

0 10 24.4 13 33.3

1 10 24.4 3 7.7

2 21 51.2 23 59.0

Total 41 100.0 39† 100.0

† It was not possible to classify the foraminal resorption in two

specimens.

Table 3 Distribution of levels of periforaminal and foraminal external

apical resorptions combined

Foraminal

Periforaminal

Level 0 Level 1 Level 2 Total

Level 0 6 (15.4%) 4 (10.2%) 3 (7.7%) 13 (33.3%)

Level 1 1 (2.6%) – 2 (5.1%) 3 (7.7%)

Level 2 3 (7.7%) 6 (15.4%) 14 (35.9%) 23 (59.0%)

Total 10 (25.7%) 10 (25.6%) 19 (48.7%) 39 (100.0%)

Apical Resorption in Teeth F. V. Vier-Pelisser et al.



using SEM, because such data inform dental professionalsof the real conditions of a tooth’s apical area.

In this experiment, 72.5% of the samples presentedsome level of radiographically visible resorption. Thisnumber stands in contrast with the findings of Laux et al.(5), where less than 20% of teeth with apical periodon-titis were diagnosed with EAR by radiographic examina-tion. Ferlini Filho (12) reported that 36.11% of samplesshowed radiographically visible resorption. Kaffe et al.

(19) described the presence of EAR in approximately50% of their samples, showing results closer to those ofthis study. However, these authors examined non-vitalteeth with and without periapical pathology and endo-dontic treatment. Based on the divergence of the resultsfound in the literature, radiographic diagnosis of EAR canbecome subjective.

In this study, radiographic images were interpreted bythree examiners in order to obtain more consistent

Table 4 Distribution of final resorption levels by SEM versus classification of radiographic analysis of external apical radicular resorption

SEM

Level 0 Level 1 Level 2 Total

Radiograph Absent 1 (2.8%) 1 (2.8%) 8 (22.2%) 10 (27.8%)

Superficial 3 (8.3%) 2 (5.6%) 14 (38.9%) 19 (52.8%)

Deep 1 (2.8%) 2 (5.6%) 4 (11.1%) 7 (19.4%)

Total 5 (13.9%) 5 (13.9%) 26 (72.2%) 36 (100.0%)

SEM, scanning electron microscopy.

(a) (b)

(c)

Figure 1 Radiograph of teeth with periapical lesions: (a) Tooth LL7 with no radiographic external apical resorption (REAR); (b) Tooth LL4 with superficial

REAR; (c) Tooth LL6 with deep REAR.




results; this procedure differs from those in other studiesusing only one examiner (5). Kendall’s coefficient ofagreement in our study was 0.6. This value is in accor-dance with that in Goldman et al. (20), which suggestedthat six examiners shared the same opinion regarding thesuccess of the endodontic treatment in less than half ofcases. The authors attribute this result to the fact thatradiographs were not read but rather interpreted. Thesefindings highlight the importance of considering the sub-jective opinions of the examiners as well as the instruc-tions given to them.

When radiographic diagnosis was used to detect peri-apical lesions, we observed using SEM that 15.4% ofsamples did not present EAR. Our findings thereforesupport those of Vier and Figueiredo (17). Ferlini Filho(12) and Laux et al. (5) used optic microscopy to reveal ahigh percentage (94.4%) of EAR in teeth with apicalperiodontitis. The similarity of these results suggest thereliability of both optical and SEM methods for the detec-tion of EAR. Both methods assess the real state of thepathologic process, despite the fact that the clinical use of

both methods is impossible. Conversely, although theradiographic exam is limited in diagnosing EAR, it is awidespread method available in many clinical routines.

The results of this study indicate that no correlationbetween REAR and SEM EAR exists. Only 19.5% of thecases showed agreement between radiographic diagnosisand SEM examination. The lack of diagnostic coincidencewas also evidenced by Laux et al. (5).

Despite the lack of correlation between REAR and SEMEAR, EAR levels measured using SEM were greater thanthose recorded by radiographic methods in 63.9% ofteeth. This finding is consistent with the results of Brynolf(10), which reported that only extensive resorptions aredetected by conventional radiographic exams.

In 16.7% of the samples, REAR was more pronouncedthan SEM EAR; this finding is not compatible with pre-viously established facts. This diagnosis error, which wasconfirmed by a radiographic exam, may be ascribed to theradiolucent quality of the periapical process partially pro-jected over the root (21). Another hypothesis involvesthe presence of medullar spaces that are misdiagnosed as

(a) (b)

(c) (d)

Figure 2 (a) Root apex with no EAR; (b–d) Root apexes with external apical resorption (EAR) and foraminal EAR present on more than 1/4 of the area

examined, showing various levels of resorption.

Apical Resorption in Teeth F. V. Vier-Pelisser et al.



resorption cavities (22). Andreasen et al. (23) pointed outthat resorption cavities located in the vestibule were pro-jected to the proximal surface when the horizontal angu-lation of the ray was changed to enhance the probabilityof a correct diagnosis.

This study shows that resorption may be present, butnot radiographically visible. This fact is important as itmay change the prognosis of treatment of teeth withasymptomatic apical periodontitis especially when den-tinal tubules become exposed allowing bacteria to furtheraffect the periapical tissues.

Conclusions

Based on our methodology, the results obtained in thisstudy suggest the following conclusions:• EARs were present in 72.5% of the radiographs andwere considered deep in 20% of cases.• With SEM analysis, periforaminal and foraminal EARoccurred in 75.6% and 66.6% of cases, respectively. SEManalysis revealed that only 15.4% of specimens werecompletely lacking EAR.• There was no correlation between radiographic diag-nosis and SEM examination when evaluating EAR.

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