Prevalence of different periapical lesions associated with human teeth and their correlation with the presence and extension of apical external root resorption

F.V.Vier&J.A.P.Figueiredo Post-Graduate Program of Dentistry, ULBRA, Canoas, Brazil

Abstract tion. The most prevalent diagnosis was noncystic peri- apical abscess with varying degrees of severity Vier FV, Figueiredo JAP. Prevalence of different periapical (63.7%). Periapical was not a frequent ¢nd- lesions associated with human teeth and their correlation with the ing. SEM analysis showed that 42.2% of the root apices presence and extension of apical external root resorption. International had periforaminal resorption extending over 50% of Endodontic Journal, 35, 710^719, 2002. their circumference. When the foraminal resorption Aim The aim of this study was to determine the pre- was evaluated, 28.7% had resorption a¡ecting >50% valence of various periapical pathologies and their of the periphery. Only 8.9% of the samples showed association with the presence and extent of apical no periforaminal or foraminal resorption. external in£ammatory root resorption in human Conclusions In the sample of extracted teeth inves- teeth. tigated, 24.5% of the periapical lesions were cysts. Most Methodology One hundred and four root apices periapical lesions (84.3%) displayed acute in£amma- from extracted teeth with periapical lesions were tion, whether cystic or not. Periforaminal resorption examined. Semi-serial sections of soft tissue lesions was present in 87.3% of the cases, and foraminal were stained with HE. The lesions were classi¢ed as resorption in 83.2%. Periforaminal and foraminal noncystic or cystic, each with di¡erent degrees of resorptions were independent entities. There was no acute in£ammation: 0, 1, 2 and 3, increasing in sever- association between external root resorption and the ity. The root apices were analysed by SEM. External nature of the periapical lesions. root resorption was classi¢ed according to site, as peri- Keywords: apical root resorption, diagnosis, periapi- foraminal or foraminal, and the extension of the cal pathology, SEM. resorbed area graded in increasing area as 0, 1, 2 or 3. Results Cysts accounted for 24.5% of the samples, 84% of which were associated with marked in£amma- Received 2 July 2001; accepted11February 2002

the periapical region (Yanagisawa 1980, Lin et al.1984). Introduction Chronic periapical lesionsbearingaproliferative charac- Following necrosis, the root-canal system ter, represented by and periapical cysts, encourages the colonization and proliferation of are the result of this process (Leonardo et al. 1998). The microbes (Estrela & Figueiredo 1999). The low intensity, slow growth of these lesions results in bone resorption chronic stimulus provided by bacteria and their pro- that is visible radiographically. ducts allows for the maintenance of in£ammation in The precise nature of such lesions can only be deter- mined histologically (Linenberg et al. 1964). However, true prevalence of each pathological conditon is unclear. Correspondence: Jose¤ Anto“ nio Poli de Figueiredo, R. Luciana de Abreu, 20/201, Porto Alegre 90570^060, RS, Brazil (tel: þ55-51-3346 2197; Cystic lesions have been reported to account for between e-mail: endo¢[email protected]). 3.2% (Nair 1987) and 54% (Priebe et al. 1954) of apical

710 International Endodontic Journal, 35, 710^719, 2002 ß 2002 Blackwell Science Ltd Vier & Figueiredo Apical lesions and resorption lesions, and granulomas for between 45% (Lalonde & sections (0.5 m at 0.5-mm intervals) of soft periapical Luebke 1968) and 96.8% (Nair 1987). Some of this may lesions were stained with HE.The periapical lesionswere be explained bydi¡erences in sample source and histolo- classi¢ed as: gical methods. Noncystic lesions A number of chemical mediators of in£ammation,  Periapical granuloma: Lesions predominantly in¢l- including the cytokynes IL-1a,IL-1b,TNFa, prostaglan- trated bylymphocytes, plasmacells and , dins and LPS, seem to be related to the pathogenesis of with or without epithelial remnants (Nair et al. 1996), periapical lesions (Schein & Schilder 1975, Schonfeld and covered by a capsule of collagen ¢bres. In these et al. 1982, Burchett et al. 1988, Wang & Stashenko lesions, neutrophils were sparse forming no abscess 1993a,b). These substances may stimulate root resorp- microcavities or concentrated in¢ltrates. tion in the same way that they stimulate bone resorption  Periapical abscess: Lesions with a distinct collection of (Hammarstro« m & Lindkog1992). neutrophils in the interior of a previously existent Although radiographic examination is an important granuloma (Nair et al.1996). These were further cate- resource in clinical diagnosis, it is rarely helpful in the gorized as 1 ¼ abscess cavity occupying up to one- diagnosis of small areas of external root resorption asso- third; 2 ¼1/3^2/3; 3 2/3 of the total area of the ciated with teeth having apical periodontitis (Bhaskar visualized lesion in the histological sections. & Rappaport1971, Ferlini Filho1999, Laux et al. 2000). Cystic lesions Irregularresorbedareasarefrequentlysituatedinsites  : Lesions with a layer of strati¢ed squa- that are not within the reach of root-canal instruments mous epithelium along a surface of su⁄cient quantity or medication and may act as niches for extraradicular of conjunctive tissue to indicate a delineated cavity bacterial colonization (Tronstad et al.1990,Lomc¸ali and surrounded by a slight ¢brous capsule (Patterson et al.1996), besides causing technical problems for root- etal.1964, Lalonde & Luebke1968,Lalonde1970,Nobu- canal treatment (Delzangles1989, Malueg et al. 1996). hara & Del Rio1993,White et al.1994). There are few reports correlating periapical lesions  Abscessed periapical cyst: Cysts containing pus-¢lled with external in£ammatory root resorption (Delzangles cavities were classed as1,2 or 3 as above. 1989, Bohne 1990, Vier & Figueiredo 2000). The aim of The histological sections were analysed by two this study was to evaluate the prevalence of di¡erent blinded and previously calibrated observers, using 32, periapical lesions as well as to evaluate the presence 100 and 400 magni¢cation (Zeiss microscope, Thorn- and extension of apical external resorption and its asso- wood, USA). ciation with di¡erent categories of disease. The diagnosis of each lesion was determined by con- sidering all the histological sections. The presence of epithelium delineating a pathological cavity in one or Materials and methods more sections of a lesion characterized it as a periapical The sample comprised 113 extracted human teeth with cyst. Classi¢cation of abscess severity was based on the visible periapical lesions. These extracted teeth were section showing its largest dimension. Thereafter, the obtained from the Public Dental Services in the state of periapical lesions were grouped in two subgroups: Rio Grande do Sul, Brazil, where endodontic or restora-  noncystic lesions: A1 ^ with absence or with a small tive treatment is not provided. Some of the teeth were abscess (periapical granuloma and abscess degree 1); symptomatic, others were removed because the crown A2 ^ with advanced abscess (periapical abscess was completely compromised by dental caries. Care degrees 2 and 3). was taken to include only teeth with whole and intact  cysticlesions: B1^withabsence or witha smallabscess periapical lesions. (periapical cyst and abscessed cyst degree1); B2^with The specimens were stored at room temperature in a advanced abscess (abscessed cysts degree 2 and 3). solution of formaldehyde (10%, w/v), and radiographed Theapicalportionof the root was cut perpendicular to to exclude previous root-canal treatment or incomplete thelongaxis withcarborundum disc to favourplacement root formation. Fifteen teeth were discarded, leaving a on stubs. The root apices were submerged in a solution ¢nal sample of 98 teeth, amongst which six presented of 2.5% sodium hypochlorite for 3 h, dehydrated in an two lesions on separate roots. Atotal of104 apical lesions ascending sequence of alcohols (70, 90 and 99.96%, for and104 root apices were analysed. 5 h ineach), attachedtothe stubs withtheapexupwards, The periapical lesions were gently removed from the and sputtered (Balzers, Liechtensten) with gold root apices and labelled before processing. Semi-serial palladium, to a thickness of 150 —. Scanning electron

ß 2002 Blackwell Science Ltd International Endodontic Journal, 35, 710^719, 2002 711 Apical lesions and resorption Vier & Figueiredo

microscopy was conductedusinga Philips XL 20 (Eindh- Table 1 Prevalence of di¡erent periapical lesions moven, Netherlands) microscope, operating at 15 Kv. Periapical lesion f % The areas that surrounded the apical foramina of the Noncystic lesions with absence or with 12 11. 8 apices were imaged at 100. The occu- a small degree of abscess piedthe central regionof thevideoscreenandwastotally Noncystic lesions with high degree of abscess 65 63.7 surrounded by the root. If a root presented more than Cystic lesions with absence or with a 43.9 one apical foramen, more than one image was obtained, minimum degree of abscess so as to guarantee the analyses of all the foramina. Cystic lesions with high degree of abscess 21 20.6 SEM images were analysed separately by two blinded To t a l 10 2 10 0.0 and previously calibrated observers. The dental apices were classi¢ed depending on the presence orabsence of externalapical resorption, aswell as to its extent: Table 2 Periapical lesions of minor and major severity of Periforaminal resorption: Periforaminal resorptionwas abscess de¢ned as the area of resorption not comprising the out- line of the foramen, but the surrounding area. The Type of lesion f % degrees of severity 0^3 were employed when there was A1 þB11615.7 absence of resorption, resorption of up to 1/4, from 1/4 A2 þ B28684.3 to1/2 and in more than1/2 of the area that surrounded To t a l 1 0 2 10 0.0

or circumscribed the apical foramen, respectively. A1^noncystic lesions with absence or with a small degree of abscess. Foraminal resorption: De¢ned as the resorption within A2^noncystic lesions with high degree of abscess. the outline or the perimeter of the foramen. The degrees B1^cystic lesions with absence or with a minimum degree of abscess. of severity 0^3 were employed when there was absence B2^cystic lesions with high degree of abscess. of resorption, resorption of up to 1/4, from 1/4 to 1/2 and in morethan1/2 of the areaof the outline or theperi- meter of the apical foramen, respectively. Table 3 Extension degrees of periforaminal and foraminal Whenever a tooth presented with two or more apical resorption of the dental apexes foramina or had fused roots, the degree of ¢nal resorp- Resorption tion measured was the foramen where the resorption Periforaminal (PR) Foraminal (FR) was most severe. Degree of Kappa coe⁄cient was employed to evaluate the degree resorption f% f % of agreement amongst the examiners, both in diagnos- 01312.71716.8 ing the periapical lesions and in the presence and exten- 1 15 14.7 25 24.8 sion of periforaminal and foraminal external resorption. 23130.43029.7 Theanovastatisticaltest was used toevaluatethe cor- 34242.22928.7 relation between the histopathological diagnosis of the To t a l 10 2 10 0.0 10 1 10 0.0 periapical lesions and the presence and extension of In one specimen, it was not possible to perform a classification of the the external apical root resorption, followed by the Dun- foraminal resorption. can test of multiple comparisons. Due to the ordinal nat- ure of the data, the Kruskal^Wallis anova was also used. The frequencies observed in the groups were com- pared using the Chi-square test. Table 4 Distribution of degrees of periforaminal and foraminal resorption combined Results Foraminal (FR) Periforaminal (PR) 0123Total

Histopathology 0 921113 The results are presented in Tables 1^5. Analysis was 1355215 2 31015331 completed in a total of 102 specimens, as two were 3 2 8 9 23 42 lost during preparation. The degree of agreement Total 17253029101 amongst the observers concerning the diagnosis of the

712 International Endodontic Journal, 35, 710^719, 2002 ß 2002 Blackwell Science Ltd Vier & Figueiredo Apical lesions and resorption

Table 5 Median (p25^75) of the degrees Resorption of periforaminal and foraminal resorption according to the di¡erent Periforaminal (PR) Foraminal (FR) periapical lesions Periapical Lesion n md p25^p75 md p25^p75

A1 12 2.0 2.0^3.0 2.0 1.5^2.0 A2 65 2.0 1.0^3.0 2.0 1.0^3.0 B1 4 2.0 0.5^3.0 1.0 0.5^2.0 B2 21 2.0 1.0^2.0 1.0 0.0^2.0

Periforaminal: P ¼ 0.227; foraminal: P ¼ 0.163. A1^noncystic lesions with absence or with a small degree of abscess. A2^noncystic lesions with high degree of abscess. B1^cystic lesions with absence or with a minimum degree of abscess. B2^cystic lesions with high degree of abscess. In one specimen, it was not possible to perform a classification of the foraminal resorption.

periapical lesions gave a Kappa coe⁄cient of 0.96 (IC Periapical cysts represented 24.5% of the sample. Just 95 % ¼ 0.82^1.0). four (3.9%) periapical cysts presented with no or small Periapical granuloma was not a common ¢nding. A1 abscess cavities (Fig. 2). Amongst the 25 cysts analysed, lesions (granuloma and periapical abscess score1) com- 21 (84%) had large abscess cavities.The abscessed areas prised only11.8% of the sample (Table 1).The most preva- were associated with an epithelial component resulting lent histological diagnosis was the lesions classi¢ed as in disorganization and discontinuity. The greater the A2 (noncystic periapical abscess scores 2 and 3) severity of the abscess, the bigger the epithelial disinte- (Fig. 1), which comprised 63.7% of the sample (Table 1). gration observed. In other cases, the cavities of the

Figure 2 Periapical cyst (cystic lesion with the absence of Figure 1 Periapical abscess degree 3 (14). abscess microcavities) (32).

ß 2002 Blackwell Science Ltd International Endodontic Journal, 35, 710^719, 2002 713 Apical lesions and resorption Vier & Figueiredo

de¢ned abscess in that site. Disregarding the cystic characteristic of the lesions and by just analysing the presence of an abscess, we were able to observe that 86 lesions (84.3%) had abscess cavities that occupied a large area. Just 16 lesions (15.7%) were free from or contained only microcavities of acute in£ammatory cells (Table 2).

Resorption Only 12.7% of the samples were free of periforaminal resorption and 16.8% showed integrity of the foraminal surroundings (Table 3). From all the samples, 72.6% had periforaminal resorption, reaching more than 1/ 4th of the area around the foramen (Fig. 4). Moreover, in 42.2% of these cases, the resorption included more than half of this area (Fig. 5).When foraminal resorption occurred, 58.4% of the samples were a¡ected in more than 1/4 of their perimeter (Fig. 6), and 28.7% in more than half (Fig. 7). Just 8.9% of the samples had no resorp- tion (Table 4). FromTable 4, it is clear that the pattern of periforam- inal resorption did not depend on the pattern of foram- inal resorption or vice-versa. An apex may present with substantial periforaminal resorption, without Abscessed cyst degree 3, with abscessed area Figure 3 alteration to the foramen. The apical foramen may be adjacent to the epithelial component (14). resorbed, even if the zone that surrounds it had an intact cementum structure. However, the resorption could abscesses were situated mainly on the connective tissue occur both in a periforaminal and foraminal location adjacent to the epithelial layer (Fig. 3). and to di¡erent degrees. There were cases where focal areas of neutrophils By associating the presence of periforaminal and for- were absent within the cyst epithelium in one histologi- aminal resorption, we were able to perceive that 49.5% cal section, but the following section often revealed a of the apices had resorption in more than 1/4th of the

Figure 4 Apex with periforaminal resorption involving1/4^1/2 of the area. Pronounced areas of lacunae (A). Interlacunae crests were not much evident (B) (PR:2; FR:2; lesion: B2) (100).

714 International Endodontic Journal, 35, 710^719, 2002 ß 2002 Blackwell Science Ltd Vier & Figueiredo Apical lesions and resorption

Figure 5 Apex with periforaminal resorption involving more than half of the radicular surface examined.The resorption displayed a honeycomb aspect (PR:3; FR:3; lesa‹ o: A2) (100).

Figure 6 Apex with foraminal resorption involving1/4^1/2 of the perimeter with a not well de¢ned, or even absent outline of the interlacunae crests (PR:1; FR:2; lesion: B2) (100).

examined area, and in more than half in 22.8% of cases cementum surface orbya set of interconnected gapsthat (Table 4)(Fig. 7). The lacunae of resorption were similar were occasionally related to other resorption zones. to the Howship type, showing a circular shape of di¡er- Sometimes, the apex had fused areas of resorption, and ent sizes.The combination of various lacunae resembled was totally deprived of intact cementum (Fig. 5). There the characteristic aspect of honeycombs (Fig. 5). Gener- were cases with evidence of exposed dental tubules ally,the areas of resorption were superimposed, project- (Fig. 8), demonstrating sites of increased resorption. ing pronounced margins (Fig. 4). However, in some The foraminal resorptionviewed by SEM followed two cases, due to the fusion of the lacuna, or due to its shal- peculiarcharacteristics. Insome apices, therewas defor- lowness, the interlacunae crests became less obvious mation of the original foramen outline, due to deep or even absent (Figs 4 and 6). resorption, though in very speci¢c places (Fig. 9). In The resorbed areas resulted in the presence of one others, although the apical foramen had not su¡ered or two isolated lacunae, surrounded by an integral visible morphological alterations, it was possible to

ß 2002 Blackwell Science Ltd International Endodontic Journal, 35, 710^719, 2002 715 Apical lesions and resorption Vier & Figueiredo

Figure 7 Apex with periforaminal and foraminal resorption involving more than half of the radicular surface examined (PR:3; FR:3; lesion: A2) (100).

Figure 8 Apex with extensive periforaminal and foraminal resorption exposing dentinal tubules (PR:3; FR:2; lesion: A2) (100).

Figure 9 Apex with foraminal resorption with morphological alterations of the apical contour (PR: 3; FR:3; lesion: A2) (100).

716 International Endodontic Journal, 35, 710^719, 2002 ß 2002 Blackwell Science Ltd Vier & Figueiredo Apical lesions and resorption observe shallow resorption gaps, surrounding the Di¡erences in histological criteria create di⁄culty in majority of its outline (Figs 5 and 8). comparing similar studies (Langeland et al.1977, Spata- According to Table 5, we can verify that there was no fore et al.1990, Nobuhara & del Rio 1993). Our study, for statistically meaningful di¡erence between the type of example, demonstrated an unusually low prevalence of periapical lesionand the degree of periforaminaland for- periapical granuloma and high prevalence of noncystic aminal resorption at the root apex. abscesses. This may be due to the sample, which con- sisted of teeth extracted in the Public Oral Services in poor areas in southern Brazil, where the presence of Discussion symptoms is one of the main reasons for dental visits. Many teeth with apical periodontitis are believed to The prevalence of 24.5% of cystic lesions is in accord show some degree of external periapical resorption, with previous reports (Linenberg et al. 1964, Langeland but few studies have related resorption with the nature et al. 1977, Nobuhara & del Rio 1993,White et al.1994). of the apical lesion (Delzangles 1989, Bohne 1990, Vier However, when evaluating other studies with similar & Figueiredo 2000). This study sought to address this methodology, i.e. lesions associated with the apices of issue by correlating periapical pathology with the pre- extracted teeth, the results were higher than the 17 sence and extension of periforaminal and foraminal and15% of the cysts diagnosed by Simon (1980) andNair resorption. et al. (1996) respectively. The results were closer to the Thepresenceofperiapicalpathosiswasdeterminedby 28% reported by Linenberg et al. (1964), whose samples direct visualization of root apices (Linenberg et al. included material curetted from extraction sockets and 1964, Simon 1980, Garrocho & Antonio Neto 1984, Nair lesions associated with extracted teeth. 1987, Bohne1990, Nair et al.1996). Radiographic exami- This study also evaluated the extension of resorption nation was not conducted prior to tooth extraction. over the apical root surface. The results are di⁄cult to The presence of a periapical radiolucency does not correlate with manyothers who simply reported the pre- necessarily indicate periapical in£ammation, other sence of resorption on the root surface (Simon et al. causes may include apical scar tissue (Nair et al. 1999). 1981, He s s et al.1983, Laurent-Maquin et al. 1986, Delzan- Conversely, a periapical in£ammatory reaction of endo- gles 1989, Bohne 1990, Lomc¸ali et al.1996,Bonifa¤ cio dontic origin may exist without being visible radiogra- et al. 2000). phically (Bender & Seltzer1961). From the methodology employed, 8.9% of specimens Semi-serial sections were performed on the speci- had no periforaminal or foraminal resorption, despite mens, since abscess cavities or even the epithelial lumen pulp necrosis and periapical lesions. These results are of a cystic cavity may be away from the centre of the spe- in agreement with those of Henry & Weinmann (1951) cimen or from the place elected for randomized sections and Ferlini Filho (1999) who reported that10% of their (Garrocho & Antonio Neto 1984), a fact which could specimens had no resorption. make it di⁄cult to reach the ¢nal diagnosis. The most Apical periodontitis is amongst the causes of progres- accurate analysis is achieved from serial sectioning of sive in£ammatory resorption cited by Soares & Goldberg intact lesions. (2001). Nevertheless, it is impossible to determine the We classi¢ed abscesses as lesions without epithelium in£uence of other factors that might potentiate resorp- in the body of the lesion and with a massive accumula- tion such as occlusal trauma. We had no access to tion of neutrophils. The lesions diagnosed as periapical detailed medical or clinical data to control for such para- granulomas exhibited neutrophils, though not forming meters. distinctarrangements or inadegeneratingstate.Weclas- Theapical resorptionobserved inthepresent studydid si¢ed cysts according to Patterson et al. (1964), Lalonde not di¡er amongst the various periapical pathological & Luebke (1968), Lalonde (1970), Nobuhara & del Rio conditions, sinceallof themexhibitedacommonfeature, (1993) and White et al. (1994), because when cysts i.e. the presence of in£ammation. This is an important become infected the epithelium may not be complete aspect to consider in the histological description of or intact, but disintegrated in some areas. these cystic and noncystic lesions, independent of the Afterathoroughand individualanalysis of eachhisto- degree of abscess. Bothconstitute a continuous andvari- logical section, we agreed with Linenberg et al.(1964), able aspect of the same phenomenon, in£ammation. who demonstrated transitional stages between one type The physical presence of a periapical lesion could pro- of lesion and another when analysing various histologi- mote root resorption in addition to bone lysis, as it makes cal sections of the same lesion. room for its organization and growth, independently of

ß 2002 Blackwell Science Ltd International Endodontic Journal, 35, 710^719, 2002 717 Apical lesions and resorption Vier & Figueiredo

its histological classi¢cation. Thus, the results of the Bhaskar S, Rappaport H (1971) Histologic evaluation of endo- present study di¡er from those of Delzangles (1989) dontic procedures in dogs. Oral Surgery, Oral Medicine and and Vier & Figueiredo (2000), who included a small Oral Pathology 31, 526^35. number of cystic samples and used less re¢ned histolo- Bohne W (1990) Light and ultrastructural studies of human chronic periapical lesions. JournalofOralPathologyandMed- gical sectioning. icine19,215^20. Normally,the failure of root-canal treatment is related Bonifa¤ cio K, Leonardo M, Rossi M, Silva L, ItoI (2000) MEV^ ava- to the persistence of infection in the root-canal system liac¸a‹ odoa¤ pice root de dentes de humanos com e sem vitali- (Sjo« gren et al. 1997, Sundqvist et al. 1998). The presence dade pulpar. (Abstract A217) Pesquisa Odontontolo¤ gica of root resorption in teeth with periapical lesions is Brasileira14 (Suppl.), 87. important for infection control since these areas are Burchett S,WeaverW,Westall J, Larsen A, Kronheim S,Wilson C niches for bacteria. Moreover, the apical limit of instru- (1988) Regulation of tumor necrosis factor/cachectin and mentation may be altered in teeth with widely resorbed IL-1 secretion in human mononuclear phagocytes. Journal apices, since the cementum^dentine junctionat the con- of Immunology140, 3473^81. striction can be missing (Delzangles 1989, Malueg et al. Delzangles B (1989) Scanning electron microscopic studyof api- 1996). In such circumstances, sealing the canal may be cal and intracanal resorption. Journal of Endodontics 15, 281^5. di⁄cult and over¢lling is likely. Estrela C, Figueiredo J (1999) Endodontia: princ|¤ pios biolo¤ gicos e Bacteria may also be found in the external surface meca“ nicos,1stedn.Sa‹ o Paulo, SP, Brazil: Artes Me¤ dicas, pp. of the root, forming a periapical bio¢lm (Leonardo & 191^245. Silva 1998), thus con¢rming the importance of appre- Ferlini Filho J (1999) Estudo radiogra¤ ¢co e microsco¤ pico das ciating the existence of periforaminal root resorption. reabsorc¸o‹ es radiculares na presenc¸a de periodontites apicais No bacterial bio¢lms were, however, demonstrated in cro“ nicas (microscopiao¤ ticae eletro“ nica devarredura).Thesis. this study. Sa‹ o Paulo, Brazil: Universidade de Sa‹ o Paulo. GarrochoA, Antonio Neto M (1984) Da relac¸a‹ o entre a cavidade do cisto rad|¤ culo denta¤ rio com o forame apical. Arquivos Do Conclusions Centro de Estudos Da Faculdade de Odontologia Da UFMG 21, On the basis of our study of extracted human teeth, we 95^100. Hammarstro« m L, Lindkog S (1992) Factors regulating and mod- conclude that: ifying dental root resorption. Proceedings of the FinnlandDen-  Cystic lesions accounted for 24.5% of chronic periapi- tal Society 88 (Suppl.1),115^23. cal lesions; Henry J,WeinmannJ (1951) The pattern of resorption and repair  The majority of chronic periapical lesions (84.3%), of human cementum. Journal of theAmerican Dental Associa- whether cystic (20.6%) or noncystic (63.7%), had large tion 42,270^90. collections of acute in£ammatory cells; HessJ,CulierasM, Lamiable N (1983)Ascanningelectronmicro-  Periforaminaland foraminal resorptions werepresent scopic investigation of principal and accessory foramina on in 87.3 and 83.2% of roots associated with periapical the root surfaces of human teeth: thoughts about endodontic lesions; pathology and therapeutics. Journal of Endodontics 9, 275^81.  The pattern of periforaminal resorption was indepen- Lalonde E (1970) A new rationale for the management of peria- dent of the pattern of foraminal resorption; pical granulomas and cysts: an evaluation of histhopatholo- gical and radiographic ¢ndings. Journal of the American  There was no correlation between the histopathologi- Dental Association 80,1056^9. cal diagnosis of the periapical lesion and the presence Lalonde E, Luebke R (1968) The frequency and distribution of and extension of apical external root resorption. periapical cysts and granulomas. Oral Surgery, Oral Medicine, Oral Pathology 25,861^8. Acknowledgements Langeland K, Block R, Grossman L (1977) A histopathologic and histobacteriologic study of 35 periapical endodontic surgical This study was sponsored by CNPq, Brazilian Research specimens. Journal of Endodontics 3,8^23. Institute. Laurent-Maquin D, Blocquaux Verchere M, Bouthors S (1986) Modi¢cations morphologiques radiculaires de dents atteintes ¤ References d’une le¤ sion pe¤ riapicale. Etude au microscope e¤ lectronique a' balayage. Revue d’Odonto-Stomatologie 15,379^84. Bender I, Seltzer S (1961)Roentgenographic and direct observa- Laux M, Abbott P,Pajarola G, Nair P (2000) Apical in£ammatory tion of experimental lesions in bone: I. Journal of theAmerican root resorption: a correlative radiographic and histological Dental Association 62,152^60. assessment. International EndodonticJournal 33,483^93.

718 International Endodontic Journal, 35, 710^719, 2002 ß 2002 Blackwell Science Ltd Vier & Figueiredo Apical lesions and resorption

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