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Healing after removal of benign cysts and tumors of the jaws

A radiologic appraisal
Tadahiko Kawai, DDS, PhD, a Shumei Murakami, DDS, PhD?
Hiroko Hiranuma, DDS, c and Masayoshi Sakuda, DDS, PhD, d Osaka, Japan
OSAKA UNIVERSITY, FACULTY OF DENTISTRY

A retrospective review of the radiographic findings after removal of benign jaw cysts (n = 31) and ameloblastomas
(n = 24) was carried out. The radiographic features of the site margins and interior contents were classified into four categories.
In most patients radiographic changes were detected between 1 and 4 months after removal of the lesion, and complete bone
healing was found 4 months or more after surgery. Radiographic changes included "spiculed" or "trabecular" contents within
the interior of the surgical site. The fourth month was found to be the optimum time for follow-up radiographic examination for
the early detection of residual lesions. In nine (53%) of the patients who had ameloblastoma, recurrent lesions were noted
within or at the periphery of the original surgical sites 6 to 10 years after the initial tumor removal. (ORALSURGORAL/IVIEDORAL
PATHOLORALRADIOLENDOD1995;79:517-25)

Whereas the local recurrence rate and time to recur- moval of benign jaw cysts or tumors generally de
rence after removal of ameloblastoma have been scribe small samples of patients or of even single in-
evaluated and described,Ill the treatment choices for dividuals. Additionally most of these reports have il-
ameloblastoma remain controversial. 14,12q7 The lustrated only the final result of bone healing by
long-term elimination of ameloblastoma has not been radiographs obtained years after surgery and have not
completely successful regardless of the treatment. For described the early stages of the healing process in
surgery the recurrence rate is about 10% for the uni- detail), 7, 9, 11, 17, 18, 40-45 To our knowledge no report
cystic type of this tumor when it is treated by enucle- has described the radiographic alterations observed at
ation and curettage, and the recurrence rate is 50% to various time intervals throughout the entire process
90% in ameloblastomas in general.2"7 Nevertheless until complete healing after removal of such benign
enucleation with curettage still remains a treatment lesions. To study the radiographic features of bone
of choice for patients with unicystic ameloblasto- healing, we conducted the present retrospective re-
ma,5, 13, 14, 16, 18 and enucleation with marginal resec- view of radiographs made after the removal of benign
tion of healthy bone is recommended for young jaw cysts and ameloblastomas. The purpose was to
patients with ameloblastoma regardless of the histo- investigate radiographic alterations at specific time
logic pattern. 2, 4 The follow-up program for patients intervals throughout the entire healing process until
who have such tumors should include monitoring for complete bone healing occurred. This study was also
the early detection of recurrence in an effort to reduce conducted to determine the optimum time of fol-
morbidity and medical expense. low-up examination after surgery for the early detec-
Although animal experiments and clinical studies tion of retained, residual, or recurrent lesions.
have thoroughly elucidated the histologic condition
and biochemistry of healing after bone injury, 19-29 MATERIAL AND METHODS
relatively few reports have described the radiology of The 55 patients included in this study had been
postsurgical bone healing in animals and humans, 28"39 treated for dentigerous cyst (13), odontogenic kera-
and even fewer have described the radiographic tocyst (18), and ameloblastoma (24) by fenestration,
alterations during the healing process after conserva- currettage, or enucleation at Osaka University Den-
tal Hospital during the past 10 years (Table I).
tive removal of benign jaw lesions. Furthermore the
Patients were excluded, if they had secondary infec-
few clinical reports describing bone healing after re-
tion, if they were lost to follow-up examination, or if
the radiographic image quality was poor.
aDepartment of Oral and Maxillofacial Radiology. A total of 374 follow-up radiographs including
bDepartment of Oral and Maxillofacial Radiology. panoramic (n = 178), posteroanterior skull (n = 175),
CDepartment of Oral and Maxillofacial Radiology.
dprofessor, Department of Oral and Maxillofacial Surgery. lateral oblique projection of the mandible (n = 13),
Copyright | 1995 by Mosby-Year Book, Inc. panagraphs (n = 4), and occlusal radiographs (n = 4)
1079-2104/95/$3.00 + 0 7/16/60705 were reviewed from the selected 55 patients. The ra-
5/7
518 Kawai et al. ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
A p r i l 1995

Table I. The study population

~ ibuao.

patients Male Female (yr) SD

Odontogenic 31 20 11 28.6 18.6


cyst
I. unchanged H. slightly changed Ameloblastoma 24 16 8 25.7 12.7

diographic features of the lesion margin and of the


internal portion of the postsurgical area were evalu-
ated on the basis of the criteria illustrated in Figs. 1
and 2.
The postsurgical radiographic pattern of the surgi-
cal margins in patients who had odontogenic cysts and
ameloblastomas was classified as unchanged when the
III. partly reduced IV. entirely absent original radiopaque margin of the lesion was unal-
Fig. 1. Diagramatic representations of radiographic fea- tered, slightly changed when the clarity and width of
tures of surgical site margin observed during course of bone the original margin were reduced, partly reduced
healing after removal of odontogenic cyst or ameloblas- when the clarity of the original margin was decreased
toma. Original cystic margin is I, completely preserved; II, or when the original margin had partially disappeared
partly decreased in width and clarity; III, partly absent; and or was partly displaced inward toward the center of
IV, entirely absent. the surgical area, and entirely absent when the entire
margin of the lesion was completely absent (Fig. 1).
The postsurgical radiographic appearance of the

~
internal portion of the surgical site was classified as
unchanged when no change from the presurgical ap-
pearance was observed, "ground glass" when a slight
increase in radiopacity was noted, spiculed when bone
X spicules were visible from the periphery to the center
X
of the site, and trabecular when radiating trabeculae
X
X enclosing marrow spaces were observed (Fig. 2).
H. ground glass appearance When both ground glass appearance and spicules
were observed at the same surgical site, the radio-
graphic appearance was categorized as "spiculed"
because of the more calcified feature. When both sp-
icules and trabeculation were observed at the same
surgical site, the appearance was classified as "tra-
becular" for the same reason. "Trabecular" as used
here does not always indicate "complete bone heal-
ing" but rather a stage in the bone healing process.
The features of the presurgical and postsurgical ra-
X
III. spiculed IV. trabecular diographs in six patients are illustrated in Figs. 3 to 8.
All of the radiographs in this study were evaluated
Fig. 2. Schematic drawings of radiographic features of by three of the authors independently. Each was
interior of surgical site observed during course of bone blinded to the time interval the radiograph was taken
healing after removal of odontogenic cyst or ameloblas- after surgery. The images at recall and baseline were
toma. I, Unchanged; radiographic features of internal
viewed and compared side by side. When a marked
surgical site show no change after operation. II, Ground
glass appearance; periphera ! portion of surgical site shows density difference between presurgical and postsurgi-
ground glass appearance. III, Spiculed; radial bone spic- cal radiographs was noted, comparison of the images
ules are found in peripheral portion. IV, Trabecular; surgi- was performed with a variable intensity light.
cal site is regenerated with normal cancellous bone archi- For radiologic tracking of the progression of site
tecture. healing after conservative removal of benign lesions,
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Kawai et al. 519
Volume 79, Number 4

Fig. 4. Panoramic view in patient with dentigerous cyst


involving left upper lateral incisor, a, Presurgical radio-
Fig. 3. Panoramic radiographs in patient with dentigerous graph showing uniform radiolucency with well-defined
cyst patient, a, Presurgical panoramic radiograph reveals margin, b, Two-month postsurgical panagraphy showing
well-defined radiolucency including left lower second mo- bony spicules in peripheral portion of surgical site (white
lar. b, Two-month postsurgical panoramic radiograph show- arrows).
ing ground glass appearance along inferior border of surgi-
cal site (white arrows). Ghost image, more radiopaque zone
in ascending ramus of mandible, is clearly visible, but does test analysis of the incidence of "unchanged" cate-
not hinder accurate interpretation of this image. gory in this period. The results shown in Table III in-
dicate that the high incidence of the "unchanged"
we analyzed the occurrence of radiographic changes category is significantly associated with this period
in the margin and interior of the surgical site at spe- (p = 0.0001). It is suggested that most follow-up ra-
cific time intervals after surgery with a matched-pair diographic features in comparison with those seen
chi-squared test. immediately after surgery will not show in the first
month. Of the sites examined at 1 to 2 months after
RESULTS surgery, those categorized as "slightly changed" or
The 31 patients with od0ntogenic cyst underwent a "partly reduced" accounted for 79%, indicating that
total of 74 follow-up radiographic examinations, and the incidence of change of radiographic appearance is
the 24 patients with ameloblastoma underwent 49. high during this period (p = 0.011). Of the observa-
tions made in the second and third month after sur-
Radiographic changes in the margin of the surgical gery, 88% revealed alteration of the site margin,
site (Tables II and III) indicating that in most patients some kind of ra-
Surgical sites categorized as "unchanged" were diographic alteration will be detectable in this
observed in 21 of the 31 observations within the first period (/9 = 0.0001). Furthermore 97% of the sites
month of the postsurgical follow-up period. The "un- observed more than 3 months after surgery were
changed" category was seen in a high percentage categorized as "partly reduced" or "entirely absent,"
(68%) of the observations during the first month af- indicating that bone changes will almost always be
ter surgery (Table II). The hypothesis that radio- apparent in the site margin after a postsurgical inter-
graphic changes would not occur during the first val of more than 3 months has elapsed (p = 0.0001).
month after surgery was assessed by a chi-squared Of the observations made more than 4 months after
520 Kawai et al. ORAL SURGERYORALMEDICINEORALPATHOLOGY
April 1995

Fig. 5. Follow-upradiographs in patient with odontogenickeratocyst, a, Preoperative radiograph, b, Sec-


tion of posteroanterior skull radiograph obtained 6 months after surgery reveals regenerated bone architec-
ture excludingcentral portion of surgical site (trabecular). c, This radiograph obtained 17 months after sur-
gery reveals complete bone healing (trabecular).

Table II. Follow-up radiographic features of the surgical site margin in patients with odontogenic cyst and
ameloblastoma
Month after surgery
Radiographic Category total
categorization ~1 ~2 ~3 ~4 ~5 ~6 ---->6 (n)
Unchanged 21 1 3 1 0 0 0 26
Slightly changed 5 5 3 0 0 0 1 14
Partly reduced 5 6 7 4 0 3 1 26
Entirely absent 0 2 5 3 6 4 37 57
Month total (n) 31 14 18 8 6 7 39 123

surgery, 90% were classified as entirely absent, indi- radiographic changes would not occur during the first
cating that the site margin in most patients will month after surgery was assessed by a chi-squared
be completely remodeled during this period (p = test to analyze the incidence of the "unchanged" cat-
0.0001). egory in this period. The results shown in Table V in-
These results indicate that the follow-up radio- dicate that the high incidence of "unchanged" cate-
graphic appearance of the margin is characterized by gory is significantly associated with this period
significant progression from "unchanged" through (p = 0.0001). In other words it is suggested that most
"slightly changed" and "partly reduced" to entirely follow-up radiographic features in comparison with
absent. those seen immediately after surgery will not show
changes in the first month. Of those cases observed
Radiographic changes in the interior of the during the second month after surgery, 79% were
surgical site (Tables IV and V) classified as "ground glass" appearance or spiculed,
The "unchanged" category was seen in a high per- suggesting that newly formed bone tissues will be vis-
centage (74%) of observations made during the first ible on radiographs during the second month after the
month after surgery (Table IV). The hypothesis that operation (p = 0.0001). Of the site interiors observed
ORAL SURGERYORAL MEDICINE ORAL PATHOLOGY Kawai et al. 521
Volume 79, Number 4

Fig. 6. Panoramic radiographs in 22-year-old woman with


odontogenic keratocyst, a, Presurgical radiograph shows Fig. 7. Panoramic radiographs in patient with ameloblas-
well-defined radiolucency with sharp white lines, b, Radio- toma. a, Presurgical panoramic radiograph reveals well-de-
graph obtained 3 months and 3 weeks after surgery shows fined, expansive area of radiolucency in left lower molar to
apparent increased radiodensity of surgical site interior and ramus region, b, This panoramic radiograph obtained 6
loss of white margin. months after surgery reveals complete bone healing of sur-
gical site. Note tooth germ of left lower third molar visible
at upper area of surgical site (arrows).
in the second and third month after surgery, 75% were
classified as one of the three categories of radio-
graphic change, suggesting that in most patients some made during the first 3 months and were between
kind of radiographic alteration will be detectable in "unchanged" and "slight change" at the site margin
this period (p = 0.0001). or "unchanged" and "ground glass" appearance at
Of those site interiors observed more than 3 months the site interior. Part of the original cystic margin of
after surgery, 97% were classified as spiculed or tra- the lesion was retained in the bony healing area in sev-
becular, indicating that apparent osteogenic changes eral sites. In addition three of the surgical sites studied
will be detectable in this period (p---0.0001). Of that remained at the "trabecular" stage after a long fol-
those observed 4 or more months after surgery, 85% low-up period showed an area of incomplete healing in
were classified as showing trabecular features. This their central portion. They had a well-localized lucent
finding suggests that bone regeneration and remodel- area but did not have a clearly depicted sclerotic mar-
ing of the site will occur 4 months or more after sur- gin. These lucent areas were static for a prolonged pe-
gery (p = 0.0001). These results indicate that the fol- riod of time, ranging from 1 to several years. Increased
low-up radiographic appearance of the site interior calcification of the site interior compared with the sur-
progressed from unchanged to ground glass appear- rounding normal bone was observed in two cases. One
ance to spiculed and trabecular. The rate of interob- was observed on radiographs obtained 4 months, 17 days
server discrepancy for the three raters in radiographic after surgery, and the other was observed on radiographs
categorization was 2.4% (3 of 123) for the site mar- obtained 5 months, 23 days after surgery. However, in
gin and 1.6% (2 of 123) for the site interior. The five both sites these calcified areas had vanished within the
observations in which disagreement occurred were following 7 or 8 months.
522 Kawai et al. ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
April 1995

which hematoma, blood clots, coagulation, granula-


tion tissue, or immature fibrous connective tissue for-
mation generally develops during the first 2 weeks af-
ter surgery.2~ 2t, 25 In this study the unchanged status
sometimes persisted for up to 1 month after surgery.
This situation was probably due to the failure of ra-
diography to depict the slight initial calcification in
the wounds, which should have already been formed
histologically. The categories of "slightly changed"
and "ground glass appearance" in the site margin and
interior corresponded to the second stage of wound
healing after extraction or fracture. In this stage con-
comitant bone apposition in well-organized fibrous
connective tissues and necrotic bone resorption are
seen.19-22, 28, 29 This process develops 1 to 4 weeks af-
ter dental extractions in animals or humans and 3 to
4 weeks after fracture in humans. The features of
"slightly changed" and "ground glass" appearance
were not observed in this study until 2 months after
surgery, which is twice the interval found after dental
extraction or jaw fracture. In addition it has been re-
ported that in this stage new bone formation does not
occur randomly within the site but rather extends
from outside the marrow spaces to the socket wallzS' 26
or fracture ends. 28 It is readily apparent that these
phenomena are visualized with radiography as pe-
ripheral opacification of the site and decrease of the
site margin exactly as illustrated in the diagrammatic
representations in this article. The categories of
"partly reduced" for the site margin and "spiculed"
for the site interior correspond to the third stage o f
extraction wound or fracture healing. In this stage
bone formation develops from the wall and base of the
socket to the socket mouth, 19,21 and a hard internal
or external callus develops into' more organized bone
tissues during fracture healing.28,29 These phases
continue for 3 to 5 weeks in extraction wound
healing 19-22 and for 3 or 4 months in fracture heal-
Fig. 8. Radiographs of recurrent lesion in patient with ing. 28'29 Heppenstalles described that the average
ameloblastoma, a, Preoperative radiograph showing man- duration at the hard callus stage for major long bones
dibular ameloblastoma lesion, b, Radiograph obtained 11 in an adult was 3 to 4 months, which is consistent with
months after surgery showingcomplete local bone healing our results. The categories of entirely absent for the
of surgical site. Arrowheads indicate original surgical site site margin and trabecular for the site interior corre-
margin, e, Radiograph obtained 6 years after surgery spond to the stage of remodeling in fracture healing
showing recurrent ameloblastoma lesion (white and black in which mature bone tissues still show temporarily
arrow). increased calcification followed by remodeling of
these areas in angular deformities during the frac-
DISCUSSION ture-heating process. These calcifications and angu-
The categorization of radiologic progression used larities are ultimately remodeled into bone with nor-
in this study is compatible with the histologic phasing mal density or the original contour that existed before
of extraction wound or fracture healing previously the fractureY It is very interesting that these phe-
described in animal and clinical studies. 19"22,24-28,29 nomena have not been described in previous studies of
The category of "unchanged" in this study corre- extraction wound healing. This lack of information
sponds to the early stage of healing in such injuries in may be due to the difficulties in perceiving these phe-
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Kawai et al. 523
Volume 79, Number 4

Table IlL Radiographic progression in the site margin


Time interval
after surgery Chi-squared Degree of
Category (too) Ratio Percent analysis freedom p Value

Unchanged <1 21/31 68 50.723 1 0.0001


Slightly changed
Partly reduced 1 ~ ~ <2 11/14 79 6.471 1 0.011
Slightly changed
Partly reduced 1 < ~ <3 28/32 88 20.076 1 0.0001
Entirely absent =
Partly reduced
_->3 58/60 97 94.831 1 0.0001
Entirely absent
Entirely absent >4 47/52 90 70.275 1 0.0001

Table IV. Follow-up radiographic appearance of the surgical site interior in patients with odontogenic cyst
and ameloblastoma
Month after surgery
Radiographic Category total
categorization ~1 ~2 ~3 ~4 ~5 ~6 ->_6 (n)
Unchanged 23 3 5 0 1 0 32
Ground glass appearance 7 5 7 1 0 0 20
Spiculed 1 6 3 3 1 5 20
Trabecular 0 0 3 4 6 33 51
Month total (n) 31 14 18 8 8 38 123

Table V. Radiographic progression in the site interior


Time interval
after surgery Chi-squared Degree of
Category (mo) Ratio Percent analysis freedom p Value

Unchanged <1 23/31 74 49.978 1 0.0001


Ground glass appearance
Spiculed 1 < ~ <2 11/14 79 15.267 1 0.0001
Ground glass appearance
Spiculed 1 < ~ <3 24/32 75 15.246 1 0.0001
Trabecular
Spiculed _->3 58/60 97 72.799 1 0.0001
Trabecular
Trabecular _->4 44 / 52 85 69.113 1 0.0001

nomena because of the short time span of extraction rior converted wholely to normal trabeculae. Two
wound healing. 19-22,24-26 Difficulties may also exist in surgical sites in this study, however, showed overcal-
distinguishing the density of the healed socket, which cification of the site interior like that in the remodel-
is presumably increased, from that of the surrounding ing stage of fracture healing. Both sites showed
bone tissues, which is also overcalcified, because ini- remodeling of this feature and normal bone density
tial bone apposition is laid down in the marrow spaces about 1 year after surgery, two traits that are very
adjacent to the socket. 25, 26 Furthermore the decrease similar to the phenomena observed in the remodeling
of the socket volume in both the verticaP 9-22,24-26and stage of fracture healing.28 Based on these observa-
horizontal dimensions in patients may obscure the tions we consider that the present radiographic cate-
overcalcified density of the socket. In this study, 4 gorization of the site margin and interior after
months after surgery the overall radiographic appear- removal of benign jaw cysts and ameloblastomas is in
ance was almost the same as that of subsequent ob- general an appropriate and useful method of fol-
servations; the radiolucencies of the surgical site inte- low-up examination of patients with these diseases.
524 Kawai et al. ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY
April 1995

S u b t l e changes including either " s l i g h t l y c h a n g e d " be p e r f o r m e d every y e a r for at least 10 years after lo-
or " g r o u n d g l a s s " a p p e a r a n c e m a y not be demon- cal bone healing.
s t r a t e d without a d e q u a t e x - r a y exposure settings and
p r o p e r viewing conditions. A c c o r d i n g l y , in the evalu- REFERENCES
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Volume 79, Number 4

ride probe. ORAL SURG ORAL MED ORAL PATHOL 1991; nal rigid fixation of subcondylar fractures via an intraoral ap-
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CALL FOR REVIEWARTICLES


The January 1993 issue of ORALSURGERY,ORALMEDICINE, ORAL PATHOLOGY, ORAL RADIOLOGY,
AND ENDODONTICScontained an Editorial by the Journal's Editor in Chief, Larry J. Peterson, that called
for a Review Article to appear in each issue.
These Review Articles should be designed to review the current status of matters that are important
to the practitioner. These articles should contain current developments, changing trends, as well as re-
affirmation of current techniques and policies.
Please consider submitting your article to appear as a Review Article. Information for authors appears
in each issue of ORAL SURGERy, ORAL MEDICINE, ORAL PATHOLOGY, ORAL RADIOLOGY, AND
ENDODONTICS.
We look forward to hearing from you.

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