J Formos Med Assoc 2010;109(11):810–818

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Journal of the Formosan Medical Association Journal of the

Formosan Medical Association

Resistance of esophageal squamous cell carcinoma

Recent research advances in childhood acute lymphoblastic leukemia
Infective endocarditis at a Japanese hospital
Changes in sTREM-1 in acute respiratory distress syndrome

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Formosan Medical Association
Taipei, Taiwan

Original Article

Clinicopathological Study of 252 Jaw Bone Periapical

Lesions From a Private Pathology Laboratory
Hung-Pin Lin,1 Hsin-Ming Chen,2,3,4 Chuan-Hang Yu,5,6 Ru-Cheng Kuo,4
Ying-Shiung Kuo,4,7 Yi-Ping Wang1,3,4*

Background/Purpose: Periapical lesions are common sequelae of pulp diseases. This retrospective study
evaluated the clinical and histopathological features of periapical lesions sent to a private pathology labo-
ratory by dentists in private clinics.
Methods: Two hundred and fifty-two consecutive cases of periapical lesions were collected from
September 2005 to October 2009. Clinical data and histopathological features of these periapical lesions
were reviewed and analyzed.
Results: The 252 periapical lesions consisted of 128 periapical granulomas, 117 periapical cysts, and seven
periapical scars. These 252 lesions were taken from 252 patients (92 men and 160 women; mean
age = 43.6 years; range, 9–81 years). Of the 252 periapical lesions, 186 were found in the maxilla and 66
in the mandible. The most common site for periapical lesions was the maxillary anterior region (134 cases,
including 73 granulomas, 54 cysts and 7 scars), and the most frequently involved tooth was the maxillary
lateral incisor (64 cases, including 29 granulomas, 31 cysts and 4 scars). Of the 117 periapical cysts, 116
were lined by stratified squamous epithelium and one by mucoepidermoid epithelium. Hyaline bodies
were discovered in the lining epithelium of four periapical cysts. Odontogenic epithelial rest, cholesterol
cleft, foamy histiocytes, hemosiderin-laden macrophages, dystrophic calcification, foreign bodies, and
bacterial clumps were found in five, three, nine, two, 28, 10 and one periapical granulomas, respectively,
as well as in six, 11, eight, seven, 19, nine and eight periapical cysts, respectively.
Conclusion: Granulomas and cysts were the two most common periapical lesions. Periapical lesions occurred
more frequently in female patients and in those in their fourth to fifth decades. The most commonly
affected site for periapical lesions was the maxillary anterior region, and the most frequently involved
tooth was the maxillary lateral incisor.

Key Words: periapical cyst, periapical granuloma, periapical scar

©2010 Elsevier & Formosan Medical Association

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1
Graduate Institute of Clinical Dentistry, 2Graduate Institute of Oral Biology and 3School of Dentistry, National Taiwan
University, 4Department of Dentistry, National Taiwan University Hospital, College of Medicine, National Taiwan University,
and 7Department of Dentistry, Far Eastern Memorial Hospital, Taipei, and 5Oral Medicine Center and 6Institute of
Stomatology, Chung Shan Medical University, Taichung, Taiwan.

Received: December 18, 2009 *Correspondence to: Dr Yi-Ping Wang, Department of Dentistry, National Taiwan
Revised: January 6, 2010 University Hospital, 1 Chang-Te Street, Taipei, 10048, Taiwan.
Accepted: January 7, 2010 E-mail: [email protected]

810 J Formos Med Assoc | 2010 • Vol 109 • No 11

 Jaw bone periapical lesions

Periapical radiolucent lesions are one of the most pathology laboratories for diagnosis. A retrospec-
commonly encountered clinical findings in daily tive analysis of the periapical lesions from the
dental practice. A majority of periapical lesions archives of a private pathology laboratory can serve
are attributed to pulpo-periapical diseases and are to reflect the periapical disease profile of patients
usually managed initially by endodontic treat- and daily dental practice in private dental clinics
ment. A previous study from Taiwan has shown in Taiwan. The purpose of this study was to per-
that a total of 1,588,217 teeth were treated with form a retrospective analysis of the periapical le-
non-surgical root canal treatment in 2000.1 Within sions from a private pathology laboratory, and to
5 years after this initial treatment, 4741 received investigate further the clinicopathological features
apical surgery and 118,474 were extracted.1 As of these periapical lesions.
suggested by Nair,2 post-treatment apical peri-
odontitis refers to the failure of complete healing
of periapical alveolar bone or reduction of the Patients and Methods
apical radiolucency in root-canal-treated teeth. The
etiology of post-treatment apical periodontitis can The study group consisted of 252 cases of peri-
be either microbial or non-microbial. Microbial apical lesions retrieved from the archives of a
causes consist of intraradicular infection, actino- private pathology laboratory in Taipei, Taiwan,
mycosis and other extraradicular bacteria; whereas from September 2005 to October 2009. The tis-
non-microbial causes comprise cystic apical peri- sue specimens were sent predominantly from pri-
odontitis, cholesterol crystals, foreign bodies, and vate dental clinics and one private hospital from
scar tissue healing.2 In addition to radiolucency various regions in Taiwan. The demographic data,
of pulpo-periapical origin, various other lesions including the age and sex of the patients, and the
can occur in the periapical region; these include affected tooth were obtained by reviewing the
dentigerous cyst, cementoma, periapical cemento- pathological diagnosis requisition sheets. The up-
osseous dysplasia, periodontal diseases, traumatic per and lower jawbones were divided into three
bone cyst, non-radicular cyst, odontogenic kerato- regions: the anterior (incisor/canine), premolar
cyst, malignant tumor, and other rarities.3,4 and molar regions. The location of the lesion was
There have been inconsistent histopathologi- determined by the region in which the major
cal features in periapical lesions.5–7 The incidence part of the lesion was located. The dentists who
of cysts among periapical lesions varies greatly performed the surgical intervention were divided
from 6% to 55%, and the incidence of periapical into three vocational groups: (1) endodontists;
granulomas ranges from 45% to 94%.5 These dis- (2) other dental specialists; and (3) general dental
crepancies might be due to differences in sample practitioners.
selection, sample size, diagnosis criteria, chronic- All surgical specimens were obtained from
ity and size of the lesions, previous endodontic curettage, enucleation or extraction of the teeth
treatment, and the surgeon’s preferences.6,7 Nev- with associated periapical lesions. The specimens
ertheless, an understanding of the clinical and were fixed in 10% neutral formalin for at least
histopathological features of periapical lesions is 24 hours, dehydrated in graded alcohol, and em-
very important for daily dental practice. bedded in paraffin. The tissue blocks were cut into
In Taiwan, patients frequently seek treatment serial sections of 5 μm, and stained with hema-
in private dental clinics because of convenience. toxylin and eosin. A review of the diagnosis and
In addition to general dental practitioners, a few an analysis of the histopathological features were
specialists in various dental fields also provide ser- based on independent microscopic examination
vices in private dental clinics. Whenever dental sur- of the stained tissue sections by two oral patholo-
gical specimens are obtained in private clinics, gists. The sections with an inconsistent histopa-
they are usually submitted to one of the private thological diagnosis and findings were reassessed

J Formos Med Assoc | 2010 • Vol 109 • No 11 811

H.P. Lin, et al

using a double-headed light microscope and a Table 1. Age and sex distribution of 252 patients
consensus was reached in all cases. Emphasis was with periapical granuloma, cyst or scar*
placed on the type of epithelial lining of the cysts, Periapical Periapical Periapical
the presence of hyaline bodies of Rushton in the granulomas cyst scar
lining epithelium, and the presence of odonto- (n = 128) (n = 117) (n = 7)
genic epithelial rest, cholesterol cleft, foamy histio- Age (yr)
cytes, hemosiderin-laden macrophages, dystrophic 0–9 0 1 (0.9) 0
calcification, foreign bodies, and bacterial clumps 10–19 4 (3.1) 6 (5.1) 0
in the lesions. The types of inflammation were also 20–29 21 (16.4) 15 (12.8) 1 (14.3)
assessed. A mixed type of inflammation was de- 30–39 34 (26.6) 23 (19.7) 2 (28.6)
fined as the coexistence of both acute and chronic 40–49 32 (25.0) 29 (24.8) 2 (28.6)
50–59 20 (15.6) 22 (18.8) 0
inflammatory cells. The grade of chronic inflam-
60–69 7 (5.5) 16 (13.7) 2 (28.6)
mation was further classified as mild, moderate
70–79 9 (7.0) 4 (3.4) 0
and severe according to the extent of lympho- 80–89 1 (0.8) 1(0.9) 0
plasma cell infiltration in the tissue specimen.
Sex
Mild, moderate and severe inflammation was de- Male 39 (30.5) 50 (42.7) 3 (42.9)
fined if the extent of inflammatory cell infiltra- Female 89 (69.5) 67 (57.3) 4 (57.1)
tion was < 25%, > 25% but < 50%, and > 50% of
*Data presented as n (%).
the tissue section, respectively.
The microscopic criterion for diagnosis of
a periapical cyst included the presence of an (122) of all patients (Table 1). The mean ages of
epithelium-lined cavity surrounded by a fibrous patients with periapical granuloma, cyst and scar
connective tissue wall. The lining epithelium was were 43.1, 44.3 and 43.1 years, respectively.
further classified into stratified squamous, mu- Of the 252 periapical lesions, 186 were found
coepidermoid (stratified squamous epithelium in the maxilla and 66 in the mandible. The most
with scattered mucus-secreting cells), and respi- common site for periapical lesions was the max-
ratory types. A diagnosis of periapical granuloma illary anterior region (134 cases, including 73
was made if the lesion was composed mainly of granulomas, 54 cysts and 7 scars), and the most
fibrous or granulation tissue with various grades frequently involved tooth was the maxillary lateral
of acute and/or chronic inflammation. Prolifer- incisor (64 cases, including 29 granuloma, 31 cysts
ating odontogenic epithelium could be noted in and 4 scars). Only one periapical lesion was taken
cases of periapical granuloma. A periapical scar from the periapical area of a primary tooth (man-
was composed of a fragment of dense fibrous dibular first molar) (Table 2).
connective tissue with no or minimal chronic in- The periapical surgical interventions were
flammatory cell infiltration. mainly performed by endodontists (60.3%, 152/
252), followed by other dental specialists (31.0%,
78/252), and general dental practitioners (8.7%,
Results 22/252). Specialists other than endodontists were
predominantly oral and maxillofacial surgeons
The 252 periapical lesions consisted of 128 peri- who performed 76 apical surgery procedures and
apical granulomas, 117 periapical cysts, and seven periodontists who performed two apical surgery
periapical scars. These 252 lesions were taken from procedures.
252 patients (92 men and 160 women; mean age = Histopathological features of 128 periapical
43.6 years; range, 9–81 years). The periapical le- granulomas and 117 periapical cysts are shown in
sions occurred more frequently in patients in their Table 3. Of the 117 periapical cysts, 116 were lined
fourth to fifth decades, and accounted for 48.4% by stratified squamous epithelium (Figure 1A)

812 J Formos Med Assoc | 2010 • Vol 109 • No 11

 Jaw bone periapical lesions

Table 2. Distribution of 128 periapical granulomas, 117 periapical cysts, and seven periapical scars according
to region and tooth type*
Periapical granuloma Periapical cyst Periapical scar

Maxilla Mandible Maxilla Mandible Maxilla Mandible

(n = 100) (n = 28) (n = 79) (n = 38) (n = 7) (n = 0)

Regions
Anterior 73 (73.0) 4 (14.3) 54 (68.4) 14 (36.8) 7 (100) 0
Premolar 16 (16.0) 9 (32.1) 14 (17.7) 8 (21.1) 0 0
Molar 11 (11.0) 15 (53.6) 11 (13.9) 16 (42.1) 0 0
Permanent teeth
Central incisor 34 (34.0) 2 (7.1) 16 (20.3) 9 (23.7) 3 (42.9) 0
Lateral incisor 29 (29.0) 2 (7.1) 31 (39.2) 2 (5.3) 4 (57.1) 0
Canine 10 (10.0) 1 (3.6) 7 (8.9) 3 (7.9) 0 0
First premolar 11 (11.0) 3 (10.7) 7 (8.9) 3 (7.9) 0 0
Second premolar 5 (5.0) 5 (17.9) 7 (8.9) 5 (13.2) 0 0
First molar 9 (9.0) 12 (42.9) 9 (11.4) 9 (23.7) 0 0
Second molar 2 (2.0) 3 (10.7) 2 (2.5) 6 (15.8) 0 0
Third molar 0 0 0 0 0 0
Primary teeth
Anterior 0 0 0 0 0 0
First molar 0 0 0 1 (2.6) 0 0
Second molar 0 0 0 0 0 0
*Data presented as n (%).

and the remaining one by mucoepidermoid ep- Discussion

ithelium (Figures 1B and 1C). Hyaline bodies of
Rushton (Figure 1D) were discovered in the lin- Our study design for evaluation of periapical le-
ing epithelium of four periapical cysts. Odonto- sions was similar to that performed by Bhaskar4
genic epithelial rest, cholesterol cleft (Figure 1E), and Lalonde and Leubke.8 Bhaskar4 studied 2308
foamy histiocytes (Figure 1F), hemosiderin-laden periapical lesions from civilian endodontists and
macrophages, dystrophic calcification, foreign bod- military dentists. He found that periapical granu-
ies, and bacterial clumps were found in six, 11, loma (48%) was the most common type of peri-
eight, seven, 19, nine and eight periapical cysts, apical lesion, followed by periapical cysts (42%),
respectively, as well as in five, three, nine, two, 28, residual cysts (3.7%), and periapical scar (2.5%).
10 and one periapical granulomas, respectively Lalonde and Leubke8 evaluated 800 periapical le-
(Figures 2A–2F). Acute and chronic inflamma- sions from 134 clinicians, including dentists form
tion was noted in 36 periapical granulomas and the college of dentistry, private general dental prac-
61 periapical cysts. Chronic inflammation alone titioners, and dental specialists (predominantly
was found in 92 periapical granulomas and 56 oral surgeons). They found that 45.2% of peri-
periapical cysts, with most of them showing mod- apical lesions were periapical granulomas, 43.8%
erate chronic inflammation (Table 3). Sulfur gran- were periapical cysts, and 0.4% were periapical
ules of actinomycosis were discovered in one of scars. The results of the two aforementioned stud-
117 periapical cysts (Figures 3A and 3B). All seven ies were comparable to those of our present study.
periapical scars were composed of dense fibrous However, there existed some variations in the in-
tissue with no or minimal chronic inflammatory cidence in the other studies, which used different
cell infiltration (Figure 3C). designs from ours.6,7,9–11

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H.P. Lin, et al

Table 3. Histopathological features of 128 periapical to that (4/405) reported by Lin et al.12 The low
granulomas and 117 periapical cysts* incidence of periapical cysts associated with de-
Periapical Periapical ciduous dentition might be related to the com-
Histopathological
granuloma cyst mon ignorance of periapical radiolucency of the
features
(n = 128) (n = 117) primary teeth, and infections of pulpal and peri-
Lining epithelium apical origin in deciduous molars tend to drain
Stratified squamous 0 116 (99.1) more frequently than those in their permanent
Mucoepidermoid 0 1 (0.9) counterparts.13
Respiratory 0 0 The incidence of cholesterol clefts in periapi-
Hyaline body 0 4 (3.4) cal lesions has varied from 18% to 44%.14 In the
present study, cholesterol clefts were found in
Odontogenic epithelial rest 5 (3.9) 6 (5.1)
5.6% (14 cases) of periapical lesions. The choles-
Cholesterol cleft 3 (2.3) 11 (9.4)
terol crystals might come from disintegrating ery-
Foamy histiocytes 9 (7.0) 8 (6.8) throcytes, chronic inflammatory cells or circulating
Hemosiderin-laden 2 (1.6) 7 (6.0) plasma lipids.5 Cholesterol clefts were always sur-
macrophages rounded by foreign body giant cells. Nair5 indi-
Dystrophic calcification 28 (21.9) 19 (16.2) cated that macrophages and foreign body giant
cells are not able to eradicate the cholesterol de-
Foreign bodies 10 (7.8) 9 (7.7)
posits. It is necessary to investigate further whether
Bacterial clumps 1 (0.8) 8 (6.8) these two types of phagocytic cells have a lack of
Mixed acute and chronic 36 (28.1) 61 (52.1) enzymes to digest cholesterol, or the cholesterol
inflammation crystals are too big to engulf.
Chronic inflammation only Actinomycosis might be one of the etiologies
Mild 17 (18.5) 6 (10.7) for persistent periapical radiolucency or post-
Moderate 53 (57.6) 36 (64.3) treatment apical periodontitis. Cases of periapi-
Severe 22 (23.9) 14 (25.0) cal actinomycosis have been reported.5 Stockdale
*Data presented as n (%). and Chandler15 also showed one case of peri-
apical actinomycosis in 1108 periapical lesions,
Mucoepidermoid lining epithelium was noted which was associated with a left upper lateral
in one periapical cyst in our study. A previous incisor in a 40-year-old woman. Jeansonne16 sug-
hospital-based study from Taiwan demonstrated gested that surgical intervention to eradicate pe-
mucoepidermoid lining epithelium in three out riapical actinomycosis is necessary to cure the
of 377 periapical cysts.12 The presence of mucus- periapical lesions. Moreover, antibiotic therapy for
secreting cells in stratified squamous lining ep- 6–8 weeks is mandatory for periapical actinomy-
ithelium of periapical cysts is considered to be cosis in which infection has spread to contiguous
a process of mucous metaplasia.13 Hyaline bod- regions.
ies of Rushton were found in 3.4% of our peri- Bacterial clumps were seen in 0.8% of speci-
apical cysts. This incidence was comparable to mens of periapical granuloma and 6.9% of spec-
that (4.5%) reported by Lin et al.12 The origin of imens of periapical cyst in the present study.
hyaline bodies is considered to be a secretory prod- Except for actinomycosis, the presence of extra-
uct of odontogenic lining epithelial cells, because radicular infection is still controversial. Nair5 has
these structures are usually discovered in the lin- pointed out that microbial contamination of pe-
ing epithelium.13 riapical samples might occur because microor-
Only one of our 117 periapical cysts was asso- ganisms can aggregate around the apical foramen,
ciated with a primary tooth (a mandibular first mo- and are easily dislodged during surgery or sam-
lar). This incidence (1/117) was also comparable pling procedures. Further studies are needed to

814 J Formos Med Assoc | 2010 • Vol 109 • No 11

 Jaw bone periapical lesions

A B

C D

E F

Figure 1. Histopathological features of periapical cysts. (A) A periapical cyst lined by non-keratinized stratified squamous ep-
ithelium. (B) A periapical cyst with mucoepidermoid lining epithelium. (C) High-power view of mucoepidermoid lining
epithelium in (B) showing clear mucus-secreting cells in stratified squamous lining epithelium. (D) Hyaline bodies of Rushton
composed of linear, curved or hairpin eosinophilic structures in the lining epithelium. (E) Cholesterol clefts with some of them
being surrounded by multinucleated foreign body giant cells in the fibrous cystic wall. (F) A sheet of foamy histiocytes in the
fibrous cystic wall of a radicular cyst. (Hematoxylin and eosin stain; original magnification, A and E, 10×; B–D and F, 20×).

explore the role of extraradicular microbes other Chandler,15 but lower than that (28%) reported
than actinomyces in the pathogenesis of post- by Love and Firth10 and Koppang et al (31%).17
treatment apical periodontitis. We suggest that the majority of these foreign bod-
The overall incidence (7.5%) of foreign bod- ies were probably endodontic filling materials that
ies in periapical lesions in the present study was had been pushed beyond the apical foramen dur-
higher than that (0.4%) reported by Stockdale and ing endodontic treatment procedures.

J Formos Med Assoc | 2010 • Vol 109 • No 11 815

H.P. Lin, et al

A B

C D

E F

Figure 2. Histopathological features of periapical granulomas. (A) A periapical granuloma composed of granulation tis-
sue with a severe infiltrate of chronic inflammatory cells. (B) High-power view of (A) showing proliferating odontogenic
epithelium forming a network-like structure. (C) Cholesterol clefts with some of them being surrounded by multinucle-
ated foreign body giant cells in a periapical granuloma. (D) Aggregates of foamy histiocytes in a periapical granuloma.
(E) Cholesterol clefts and scattered hemosiderin-laden macrophages in a periapical granuloma. (F) Foreign bodies
surrounded by multinucleated foreign body giant cells in a periapical granuloma. (Hematoxylin and eosin stain; original
magnification, A, 4×; B, 10×; C–F, 20×).

Seven out of our 252 periapical lesions were root canal treatment has been described in sev-
diagnosed as fibrous scars. It is difficult to differ- eral studies.4,10,18–20
entiate inflammatory periapical lesions from scar Hull et al21 reported that 77.8% of apical sur-
tissues by evaluation of radiographs alone. Indeed, gery procedures were performed by endodontists,
misdiagnosis of the scar tissue as a sign of failed 6.6% by other dental specialists, and 15.5% by

816 J Formos Med Assoc | 2010 • Vol 109 • No 11

 Jaw bone periapical lesions

A B

Figure 3. Histopathological features of actinomycosis in a

periapical cyst and a fibrous scar. (A) A sulfur granule of
actinomycosis surrounded by a sea of polymorphonuclear
leukocytes in the cystic cavity of a periapical cyst. (B) High-
power view of (A) showing radiating actinomycotic filaments
at the periphery of the sulfur granule. (C) A fibrous scar
composed of dense fibrous connective tissue with no chronic
inflammatory cell infiltration. (Hematoxylin and eosin stain;
original magnification, A, 4×; B, 10×; C, 20×).

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