Professional Documents
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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
~ ibuao.
~
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
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
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
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
ation of r a d i o g r a p h s o b t a i n e d within 2 m o n t h s after 1. Shatkin S, Hoffmeister FS. Ameloblastoma: a rational ap-
surgery, which m i g h t reveal slight changes, a v a r i a b l e proach to therapy. ORAL SURG ORAL MED ORAL PATHOL
intensity light source is r e c o m m e n d e d . O u r d a t a sug- 1965;20:421-35.
2. Sehdev MK, Huvos AG, Strong EW, Gerold FP, Willis GW.
gest t h a t the o p t i m a l t i m e for e a r l y detection of resid- Proceedings: ameloblastoma of maxilla and mandible. Cancer
ual lesions m a y be the fourth m o n t h after surgery, 1974;33:324-33.
when r a d i o g r a p h i c changes of both the site m a r g i n 3. Adekeye EO. Ameloblastoma of the jaws: a survey of 109 Ni-
gerian patients. J Oral Surg 1980;38:36-41.
and interior are apparent. 4. Molla MR, Shaheed I, Shrestha P. Ameloblastoma: a clinical
In the evaluation of a r a d i o g r a p h o b t a i n e d 3 or study of 13 cases. Bangladesh Med Res Counc Bull 1991;17:29-
m o r e m o n t h s after surgery, a s h a r p l y defined site 35.
5. Robinson L, Martinez MG. Unicystic ameloblastoma: a prog-
m a r g i n like t h a t of the p r e o p e r a t i v e lesion m a r g i n or nostically distinct entity. Cancer 1977;40:2278-85.
a clear lucent site interior like t h a t of the original le- 6. Waldron CA. Ameloblastoma in perspective. J Oral Surg
sion l u m e n should suggest a residual lesion. W h e n 1966;24:331-3.
7. Gardner DG, Corio RL. The relation~-'-ipof plexiform unicys-
bone resorption is observed within or outside the site tic amelohlastoma to conventional ameloblastoma. ORAL
m a r g i n within this period after surgery, a s e c o n d a r y SURG ORAL MED ORALPATHOL1983;56:54-60.
infection should be suspected. A g a i n , m a r k e d d e l a y of 8. E1-Mofty SK, Gerard NO, Farish SE, Rodu B. Peripheral
ameloblastoma: a clinical and histologic study of 11 cases. J
r a d i o g r a p h i c changes m a y indicate unsuccessful sur- Oral Maxillofac Surg 199l;49:970-4.
gery, secondarY infection, or m e t a b o l i c disease. Fol- 9. Minami M, Kaneda T, Yamamoto H, et al. Ameloblastoma in
low-up r a d i o g r a p h i c features t h a t deviate from the the maxillomandibular region: MR imaging. Radiology 1992;
184:389-93.
p a t t e r n p r e s e n t e d here should be suspected to indicate 10. Thompson IOC, Ferreira R, van Wyk CW. Recurrent unicys-
residual lesion, s e c o n d a r y infection, or m e t a b o l i c dis- tic ameloblastoma of the maxilla. Br J Oral Maxillofac Surg
ease. T h e r e c u r r e n c e r a t e in our patients with amelo- 1993;31:180-2,
l 1. Collings SJ, Harrison A. Recurrent ameloblastoma? An his-
b l a s t o m a s 6 to 10 years after surgery was 53% (9 of toric case report and a review of the literature. Br Dent J
17), which is within the r e p o r t e d r a n g e for such pa- 1993;174:202-6.
tients. A persistent r a d i o l u c e n c y seen in a few patients 12. Gardner DG, Pecak AMJ. The treatment of ameloblastoma
based on pathologic and anatomic principles. Cancer 1980;
suggests t h a t such lucencies should be differentiated 46:2514-9.
f r o m t u m o r recurrence. R a d i o l u c e n c i e s t h a t precede 13. Gardner DG. Plexiform unicystic ameloblastoma: a diagnos-
b o n y h e a l i n g a r e localized in the central a r e a of the tic problem in dentigerous cysts. Cancer 198l;47:1358-63.
14. Gardner DG, Corio RL. Plexiform unicystic ameloblastoma:
site b u t a r e m a r g i n a t e d and lack clearly visualized a variant of ameloblastoma with a low-recurrence rate after
white lines in c o n t r a s t to a r e c u r r e n t lesion. Because enucleation. Cancer 1984;53:1730-5.
a m e l o b l a s t o m a has the potential for local recurrence, 15. Mtiller H, SlootWegPJ. The growth characteristics of multi-
locular ameloblastomas: a histological investigation with some
follow-up r a d i o g r a p h i c e x a m i n a t i o n should be per- inferences with regard to operative procedures. J Maxillofac
f o r m e d every y e a r for at least ! 0 years a f t e r local bone Surg 1985;13:224-30.
healing. 14 16. Leider AS, Eversole LR, Barkin ME. Cystic ameloblastoma:
a clinicopathologic analysis. ORAL SURG ORAL MED ORAL
PATHOL 1985;60:624-30.
CONCLUSION 17. Pogrel MA. The use of liquid nitrogen cryotherapy in the
A f t e r benign j a w cysts or a m e l o b l a s t o m a s a r e management of locally aggressive bone lesions. J Oral Maxil-
lofac Surg 1993;51:269-73.
removed t h e t i m e course of changes in the surgical 18. Shteyer A, Lustmann J, Lewin-Epstein J. The mural amelo-
m a r g i n parallels t h a t of the surgical site interior. T h e blastoma: a review of the literature. J Oral Surg 1978;36:866-
f o u r t h m o n t h after s u r g e r y was found to be the opti- 72.
19. Huebsch RF, Coleman RD, Frandsen AM, Becks H. The
m u m t i m e for follow-up r a d i o g r a p h i c e x a m i n a t i o n to healing process following molar extraction: I Normal male rats
e v a l u a t e w h e t h e r healing is normal. R a d i o g r a p h i c (Long-Evans strain). ORALSURGORAL MED ORALPATHOL
observation 3 or m o r e m o n t h s after surgery of s h a r p l y 1952;5:864-76.
20. Huebsch RF, Hansen LS. A histopathologic study of extrac-
defined site m a r g i n s like t h a t of the p r e o p e r a t i v e le- tion wounds in dogs. ORAL SURG ORAL MED ORALPATHOL
sion m a r g i n or of a clear lucent interior like t h a t of the 1969;28:187-96.
original lesion l u m e n m a y indicate a residual lesion. 21. Simpson HE. The healing of extraction wound. Br Dent J
1969;126:550-7.
R a d i o l u c e n c i e s associated with b o n y h e a l i n g a r e 22. Johansen JR. Repair of the postextraction alveolus in Wister
localized in the c e n t r a l a r e a of the site b u t a r e m a r - rat: a histologic and autoradiographic study. Acta Odontol
g i n a t e d without c l e a r l y visualized white lines in con- Scand 1970;28:441-6l.
23. Tsuchimoehi M, Hosain F, Engelke W, Zeicher SJ. Studies on
t r a s t to a r e c u r r e n t lesion. Follow-up r a d i o g r a p h i c focal alveolar bone healing with technetium (Tc)-99m labeled
e x a m i n a t i o n of p a t i e n t s with a m e l o b l a s t o m a s should methylene diphosphonate and gold-collimated cadmium tellu-
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY Kawai et al. $25
Volume 79, Number 4
ride probe. ORAL SURG ORAL MED ORAL PATHOL 1991; nal rigid fixation of subcondylar fractures via an intraoral ap-
71:110-5. proach. ORAL SURG ORAL MED ORAL PATHOL 1991;71:257-
24. Bodner L, Kaffe I, Littner MM, Cohen J. Extraction site heal- 61.
ing in rats: a radiologic densitometric study. ORAL SURGORAL 38. Williams MD, Pearson MH, Milner SM. Complications in
MED ORAL PATHOL 1993;75:367-72. the use of compression plates in the treatment of mandibular
25. Amler MH, Johnson PL, Salman I. Histological and his- fractures. ORAL SURG ORAL MED ORAL PATHOL 1991;72:
tochemical investigation of human alveolar socket healing in 159-61.
undisturbed extraction wounds. J Am Dent Assoc 1960;61:32- 39. Iizuka T, Lindqvist C, Hallikainen D, Mikkonen P, Paukku P.
44. Severe bone resorption and osteoarthrosis after rniniplate fix-
26. Boyne PJ. Osseous repair of the postextraction alveolus in man. ation of high condylar fractures. ORAL SURGORAL MED ORAL
ORAL SURG ORAL MEn ORAL PATHOL 1966;21:805-13. PATHOL 1991;72:400-7.
27. Amler MH. The age factor in human extraction wound heal- 40. Heimdal A, Isacsson G, Nilsson L. Recurrent central odonto-
ing. J Oral Surg 1977;35:193-7. genie fibroma. ORAL SURG ORAL MED ORAL PATHOL
28. Heppenstall RB. Fracture treatment and healing, 1st ed. Phil- 1980;50:140-5.
adelphia: WB Saunders, 1980:41-52,80-5,98-100. 41. Kerley TR, Sehow CE. Central giant cell granuloma or
29. Wilson JN. Watson-Jones fractures and Joint Injuries, 6th ed. cherubism: report of a case. ORAL SURG ORAL MED ORAL
Vol 1. London: Churchill Livingstone, 1982:14-28. PATHOL 1981;51:128-30.
30. Vose GP, Mack PB, Brown SO, Medlen AB. Radiologic 42. Eversole LR, Leider AS, Strub D. Radiographic characteris-
determination of the rate of bone healing. Radiology 1961; tics of cystogenic ameloblastoma. ORAL SURG ORAL MED
76:770-6. ORAL PATHOL 1984;57:572-7.
31. Nicholls P J, Berg E, Bliven-JR FE, Kling JM. X-ray diagno- 43. Freedman GL, Beigleman MB. The traumatic bone cyst: a new
sis of healing fractures in rabbits. Clin Orthop 1979; 142:234-6. dimension. ORAL SURG ORAL MED ORAL PATHOL 1985;
32. K/ilebo P, Strid KG. Radiographic videodensitometry for 59:616-8.
quantitative monitoring of experimental bone healing. Br J 44. Mills WP, Davila MA, Beuttenmuller EA, Koudelka BM.
Radiol 1989;62:883-9. Squamous odontogenic tumor: report of a case with lesions in
33. Marmary Y, Brayer L, Tzukert A, Feller L. Alveolar bone re- three quadrants. ORAL SURG ORAL MED ORAL PATHOL
pair following extraction of impacted mandibular third molars. 1986;61:557-63.
ORAL SURG ORAL MED ORAL PATHOL 1985;60:324-6. 45. Horner K, Forman GH, Smith NJ. Atypical simple bone cysts
34. Allard RHB, Lekkas C. Unusual healing of a fracture of an of the jaws. I: Recurrent lesions. Clin Radiol 1988;39:53-7.
atrophic mandible: report of a case. ORAL SURG ORAL MED
ORAL PATHOL 1983;55:560-63. Reprint requests:
35. Schwimmer AM, Greenberg AM. Management of mandibu- Tadahiko Kawai, DDS, PhD
lar trauma with rigid internal fixation. ORAL SURG ORAL MED Department of Oral and Maxillofacial Radiology
ORAL PATHOL 1986;62:630-7. Osaka University
36. Shufford EL, Kraut RA. Passive rigid fixation of sagittal split Faculty of Dentistry
osteotomy. ORAL SURG ORAL MED ORAL PATHOL 1989; 1-8 Yamadaoka
68:150-3. Suita City
37. Lachner J, Clanton JT, Waite PD. Open reduction and inter- Osaka 565, Japan