Ameloblastic fibroma

Ameloblastic fibroma A survey of cases from the Armed of Pathology

Forces Institute

John N. Trodahl, D.D.S., M.X.D.,* Washington, ARMED

FORCES

INSTITUTE

D. C.

OF PATHOLOGY

The ameloblastic fibroma, an uncommon odontogenic tumor traditionally considered as having both epithelial and mesenchymal components and producing no calcified dental structure, is sometimes diagnostically confused with ameloblastoma. The histomorphologic differences are now well recognized, however, and previous studies have emphasized the differences in the patterns of behavior, especially with regard to age of the patient and the more favorable prognosis as compared with that for ameloblastoma. The present study involves twenty-four acceptable cases of ameloblastic fibroma from the files of the Armed Forces Institute of Pathology. Analysis of this series essentially confirms the incidence patterns found by earlier studies but suggests that the tumor is somewhat more aggressive and has a higher potential for recurrence than is presently appreciated.

T

he ameloblastic fibroma is known as a tumor of odontogenic origin characterized by the proliferation of both epithelial and mesenchymal odontogenic tissues without the formation of hard tooth structures. As shown in Fig. 1, the epithelial (ameloblastic) component consists of islands and cords of odontogenic epithelium that often resemble the dental lamina of early tooth development. There is often sufficient differentiation of the peripheral cells of these islands, however, for recognition of characteristic high cuboidal or columnar ameloblasts. Not infrequently, the central portions of the islands resemble the stellate reticulum of the embryonic enamel organ. The mesenchymal component closely resembles the fibromyxoid tissue of the dental papilla, that is, that portion of the developing tooth bud that underlies the “cap” or “bell” of the enamel organ. Both epithelial and mesenchymal components appear to be involved in the proliferation, and for that reason the The opinions or assertions contained herein are the private views of the author and are not to be construed as official or as reflecting the views of the Department of the Army or the Department of Defense. *Staff Oral Pathologist and Veterans Administration Representative, Dental and Oral Pathology Division, Armed Forces Institute of Pathology.

547

548

Oral surg.

Trodahl

April,

1972

Fig. 1. The characteristic microscopic picture of the nmeloblastic fibroma exhibits islands and cords of odontogenic epithelium, often resembling the dental lamina of early tooth development. The stroma is a fibromyxoid, embryonic t,ype of connective tissue closely resembling the dental papilla of the developing tooth bud. (AFIP Neg. 71-4913. Hematoxylin and eosin stain. Magnification, x50.)

tumor has traditionally been classified as a member of the mized (ectodermal and mesodermal) odontogenic tumor gr0~p.l~~ Other worker+ 7 prefer to regard this group of tumors as being primarily epithelial in character with varying degrees of inductional change in the adjacent connective tissues. The most compelling reason for interest in the ameloblastic fibroma is its histomorphologic resemblance to another odontogenic tumor, the ameloblastoma. The ameloblastoma is considered an invasive, locally aggressive tumor with a high rate of recurrence. As such, it is treated with varying degrees of surgical aggressiveness, from en bloc resection to hemimandibulectomy or maxillary exenteration (depending, of course, on the extent and involvement of the tumor). In contrast, most reports and studies of the ameloblastic fibroma have supported the view that it is a nonaggressive, well-defined tumor that may be successfully treated with conservative enucleation or curettage. The purpose of this study is to report upon and analyze the cases of ameloblastic fibroma on file at the Armed Forces Institute of Pathology and to correlate our findings with those of earlier workers. In the recent literature, the comprehensive article on odontogenic tumors by Gorlin, Chaudhry, and Pindborg7 contains the most frequently quoted information on the ameloblastic fibroma. Their tabulation totals twenty-three cases, including fourteen from a review of case reports in the literature plus their series of nine cases. The observations recorded in their paper will be related and compared to an analysis of the series in the present study. METHODS

AND

MATERIALS

The files of the Armed Forces Institute of Pathology (AFIP) contain specimens and clinical data submitted by civilian sources as well as military and

Volume Number

33 4

Ameloblastic

fibroma

549

Veterans Administration hospitals. All material designated by diagnostic code as ameloblastic fibroma (or one of the terms that by earlier nomenclature included this entity, that is, soft odontoma, soft mixed odontoma, etc.) was recovered from the files. This original group of cases numbered fifty-nine. On the basis of initial review of recovered material, the number of cases acceptable for study was markedly reduced for the following reasons: (1) Six cases were rejected because either data or specimens currently recoverable were insufficient for reliable analysis. (2) Four cases were rejected because the lesions were in peripheral or soft tissues rather than being primary within bone. These cases were not considered relevant for this study. (3) Fourteen cases were rejected because the microscopic pattern was unacceptable as ameloblastic fibroma by current criteria. Some of these cases contained calcified tooth structure as part of the tumor proliferation and were more accurately diagnosed as ameloblastic odontoma. Others rejected in this group were the so-called granular cell ameloblastic fibromas and those that, because of pleomorphism and mitotic activity of the connective tissue component, were more consistent with a histologic diagnosis of ameloblastic fibrosarcoma. There were six in this category. After this preliminary review, thirty-live cases remained eligible for further study. If paraffin-blocked or wet-tissue specimens were available, step sections were prepared in order to supplement microslide material already available. Careful microscopic examination of all material was accomplished. In eleven of the thirty-five eases, microscopic foci of calcified tooth structure were identified. Since, according to strict interpretation, ameloblastic fibromas should not contain such calcified structures, our group of cases acceptable for analysis was reduced to twenty-four. The series is tabulated in Table I. These twenty-four cases were subjected to statistical analysis in order to determine patterns of occurrence relative to sex, age, race, site, presenting symptoms, type of treatment, and recurrence. In order to determine the latter, current follow-up information was requested on all cases. RESULTS The statistics on age of the present series (Table II) compare very closely with those of the cases tabulated by Gorlin, Chaudhry, and Pindborg.? The youngest patient in both series was lJ$ years of age. Their oldest patient was 39, whereas ours was 41. Seventy-one per cent of the patients in the present series were under age 20, compared with 78 per cent under 20 in their series. The average age in our series was 15.5 years ; in theirs it was 14 years. We wish to reiterate that the mean age of patients with ameloblastoma is about two decades older.8 It would appear that our study indicates a 2 :1 male-to-female ratio (Table III). Total accessions at the Armed Forces Institute of Pathology are 2.5 to 1 in favor of the male, however. Therefore, with due consideration for the population served, we conclude that there is no apparent predilection for either sex. This same conclusion was reached by Gorlin’s group. Consideration of the population served by the Armed Forces Institute of Pathology is also necessary in an analysis of occurrence by race. The ratio of

Age

at

C

c

C

C

C

M

M

M

M

M

6

-

N.S.

M

5

2%

8

6

32

12

7

7

8

9

10

11

12

M

max.

N.O.S.

mand.

mand.

Post. mand.

Ant.

---

Mand. ; N.O.S.

Post. mand.

Mand;

Ant.

Post. mand.

Ant.

Post. mand.

Post. mand.

Post. mand.

Site Post. mand.

. . ..--

N.S.

C

0

F

17

4

F

C

M

27

3

18

C

F

14

N

M

2

Race

Swelling

N.S.

N.S.

None (incidental finding on x-ray film)

X

X X

Excision

Excision Curettage Enucleation

X

of

or

block resection

re-excised

l$& yr. later, residual recurrent lesion-c/w odontoma

111yr. later,

Enucleation

Swelling, failure tooth eruption

Swelling of Enucleation

le/ls yr. later,

None (incidental finding on x-ray fdm)

Excision

re-excised

5 yr. later,

Excision

X

of

7 yr. later, re-excision; 11 yr. later, two thirds mandible resected

Swelling, failure tooth eruption

Enucleatiou and cauterization

no report

tumor found scar tissue

in

(1937-1969)

Operated”

Excision of

tenderness

2 yr. later; findings

8 yr. later; temporal

None (

Recurrence

of Pathology

Swelling

Swelling,

Enucleation

treatment

Swelling

Initial Resection of ramus and part of body

symptoms

Swelling, pain, drainage

Clinical

fibroma. Cases accessioned at the Armed Forces institute

Sex

I. Ameloblastic

Case diagnosis NO. (YTS.) 1 29

Table

follolv-up

and well

and well

and well

and well

and ~e11

and well Alive and ~vpll. Bone pattern “unusual” (in x-ray film). No frank lesion

Alive

Alive and well (after 5 yr.)

Alive

Alive

Alive

Alive

Alive

Alive and well (after 3 yr.)

Alive, psychotic, no apparent problems with jaw

No further

FOZZOW-up statxst ITo further follow-up

&

3

Q

z

Post. mand.

Post. mand.

Post. mand.

Mand.;

C

N

N

N.S.

F

F

M

M

9

15

26

6

41

19

16

17

18

19

20

21

22

23

Post. mand.

Post. mand.

C

0

Ant. and post. mand.

N.O.S.

N.O.S.

and well

Alive

Curettage

Swelling,

pain

Excision

None (incidental finding on x-ray film)

24

had been received,

Mand. = mandible;

and well

Alive

Lost to follow-up

X --

X

Enucleation

Swelling

follow-up

and well

Alive

X

Enucleation

Swelling

No further

and well

Alive

X

Excision

None (incidental finding on x-ray film)

s$a yr. later, tumor had calcified tooth structure. Diagnosis : ameloblastic odontoma lss yr. later, block resection. Diagnosis: bone with included odontoma

and well

Alive

X

N.S.

Swelling

focus

and well

residual

Alive

Excision

N.S.

M yr. later, of tumor

and well

Alive

X

Excision

Swelling

and well

Alive and well (after 4 yr.)

N.S. X

Alive

Alive! current possible resrdual or recurrent lesion, same area

Excision

7 yr. later, block resection with foci of residual tumor

N.S.

Excision

X

tenderness

Curettage

Swelling,

Swelling, some pain Excision F 21 N.S. Post. max. Ant. = anterior; Post. = posterior; Abbreviations: N = Negro; C = Caucasian; 0 = Oriental; N.S. = not stated; Max. = maxilla; N.O.S. = not otherwise specified; c/w = consistent with. *The time intervals are dated from the initial procedure in all cases. information tStatus is current unless stated “after X number of years. ” This is used in cases in which interim followup but c,urrent status was unavailable.

F

M

c

Post. mand.

C

M

3

16

M

Mand.;

c

M

9

15

N.O.S.

Max.;

N.S.

M

10

14

Post. mand.

C

F

23

13

Oral Surg. April, 1972

552

Trodahl

Table

II. Age distribution Aye (yr.l oto 10 to 20 to 30 to 40 to

No. of patients 9 19 29 39 49 Tot‘rI

Per cent

9 8 5 7 1 iT

38 33 21 4 4 iii

Youngest 18 mo. Oldest 41 yr. Median aee 15.5 yr.

Table

III. Sex distribution Patients Male Female Total

Table

No. of patients 16 8

Per cent 67 33

i-i

100

No. of patients

Per cent

IV. Race distribution Race Caucasian Negro Oriental Not stated Total

14 i 5 ii

58 13 8 21 100

accessions at the AFIP for which race is stated is approximately 84 per cent Caucasian, 9 per cent Negro, and 7 per cent other races. The distribution of the cases of ameloblastic fibroma by race in this summary (Table IV) is not a sufficient deviation from the AFIP ratio to be significant and would indicate no racial predilection. No distribution by race was recorded in the study by Gorlin and associates. The current study indicates that the ameloblastic fibroma may occur anywhere in either jaw, but most diagnosed cases have occurred in the mandible, with the highest incidence in the posterior area (Table V). This closely parallels the incidence by site reported by Gorlin’s group. By far the most frequent presenting symptom was noted to be “swelling” (Table VI). In some cases an additional symptom was also recorded. This, of course, explains the discrepancy in the total number of recorded symptoms versus the total number of cases (twenty-four). Seventeen per cent of the tumors were discovered coincidentally at the time of examination of routine dental roentgenograms. The x-ray films or comprehensive descriptions of roentgenographic findings were available in only sixteen of the twenty-four cases. On the basis of this review, the lesions varied in size from approximately 1 cm. in diameter to the lesion pictured in Fig. 2, A, which measured 8.5 cm. in greatest dimension. Nine of the sixteen radiolucent lesions could be described

Volume Number

Table

33 4

Ameloblastic

%i*

15 3 4

as both anterior

and posterior

mandible.

signs and symptoms

Sign or symptom

No. of patients 14 4

Swelling Presence on roentgenogram Pain Tenderness Failure of eruption Discharge Not stated

VII. Type of initial

Total

loo

z

Total

Treatment

18 4 4 4

: 1

“One case was recorded

Excision Enucleation Curettage Resection of jaw Not stated

li

3

Maxilla Posterior Anterior Not stated

VI. Presenting

Per cent 88 63 8

iV0. of patients

Site

Table

553

V. Site of tumor

Mandible Posterior Anterior Not stated

Table

fibroma

i 2 :

.

Per cent 58 17 13 8 8 4 21

treatment No.

of patients

12 7

Per cent 50 :i

i 1 24

i 100

as “large” (over 4 cm. in greatest dimension). A number of these, in the mandible, involved the ascending ramus and extended into the molar-premolar region. Only one case extended across the midline at the symphysis. Although most of the lesions exhibited sclerotic peripheries, three tumors compromised cortical bone. Most of the lesions (3 :l) were multilocular in character. Only the smaller ones were unilocular. Most of the lesions (3 :l) were associated with unerupted teeth. Table VII reflects the several stated types of treatment initially provided to the patients. Although different terms were used, the initial operation appeared to be conservative in all but one case. (This includes those in which the treatment was not specifically stated. The specimens available for examination in those cases gave no hint that the treatment accorded was other than conservative.) The one case in which a more radical approach was taken involved a virtual hemimandibulectomy. The roentgenogram in that case (Fig. 2, A) would indicate that the size and extent of the lesion compelled a more radical approach, especially since the surgeon was provided with an initial microscopic diagnosis of “adamantinoma.”

Oral Surg. April, 1972

Fig. d. These rentgenograms represent the clinical variation in size and progression of the lesions examined in this series. 8, This roentgenogram was taken of the excised specimen in Case 1, which had the largest lesion, measuring 8.5 cm. in greatest dimension. The photomitrogrxph shown in Fig. 1 was taken from this ease. (AFIP Neg. 71-4307-l.) B, This roentgenogram is of Case 9 and is representative of the smaller lesions encountered In the series. In this, as in most of the cases, an uneruptcd tooth was involved. (AFIP Neg. 71-4307-S.)

FOLLOW-UP As noted in Table I, some type of follow-up (current or interim) was available in twenty-three of the twenty-four cases. The duration from initial treatment to last known status ranged from 10 months to 16.5 years, with an average of 8.1 years. The follow-up information may be summarized as follows: no recurrence, thirteen cases; further procedure(s) required, ten cases. This is an apparent recurrence rate of 43.5 per cent and marks a distinct departure from the series recorded by Gorlin and associates. 7 Only two of twenty-three cases reported in their article recurred, and none of these was in their own series of nine. In the two cases that recurred, the implication was strong that these represented residual tumor rather than true recurrences. In the analysis of the present series, the clinical histories of some of the patients likewise suggest that reopcration was necessary because the original excision of the tumor was incomplete. In most, however, the initial procedure was believed to have completely removed the tumor, and yet it reappeared. In several cases the recurrent proliferation was as large as or larger than the original lesions, and more radical procedures were instituted. There was considerable variation in the microscopic features of individual tumors acceptable as ameloblastic fibroma (Fig. 3). In an attempt to find characteristics common to cases that required further treatment, all material was again carefully examined microscopically, with special attention to such variations as (1) relative predominance of stroma or epithelium, (2) differen-

Volume Number

33 4

Andoblastic

fibroma

555

Pig. 3. Some of the histomorphologic variations acceptable as ameloblastic fibroma and encountered in our series are represented by these photomicrographs. In B, the classical stroma predominates. Small islands rather than cords represent the epithelial component. (AFIP Neg. 71-4914. Hematoxylin and eosin stain. Magnification, x50.) In B, the epithelial component is in delicate nests and cords, and the stroma shows considerable hyalinization, especially prominent at the upper corners of the field. No calcified dental structures were noted, however. (AFIP Neg. 71-4915. Hematoxylin and eosin stain. Magnification, x50.) In C, there is considerable hyalinization around the epithelial islands. The stroma shows increased cellularity and increased fibrosis. (AFIP Neg. U-4916. Hematoxylin and eosin stain. Magnification, x56.) In D, there is increased cellularity of the stroma and increased size and prominence of the epithelial component? with some differentiation of stellate reticulum. (AFIP Neg. 71-4917. Hematoxylin and eosm stain. Magnification, x50.) In E, the differentiation of stellate reticulum of the stroma is is increased, the epithelial component is prominent? and the vascularity increased. (AFIP Neg. 71-4312. Hematoxylin and eosm stain. Magnification, x50.) In F, there are prominent acanthomatous changes in two of the epithelial islands. Such acanthomatous changes were seen in two cases, both from recurrent lesions (one after 11 years, the other after 7 years). (AFIP Neg. 71-4309. Hematoxylin and eosin stain. Magnification, x50.)

556

Trodahl

Oral Surg. April, 1972

tiation of the epithelium, (3) amount and character of the “inductive effect,” (4) cellularity of stroma, and (5) vascularity of stroma. In like manner, the series was evaluated for a common denominator of age, sex, race, site, or roentgenographic appearance. All such efforts were unfruitful. The inference, on this basis, is that there a.re no reliable criteria that may be used to estimate the potential for recurrence of a given case of ameloblastic tibroma. DISCUSSION It is evident from the foregoing that, with the exception of follow-tip results, an analysis of the cases of ameloblastic fibroma from the files of the Armed Forces Institute of Pathology closely parallels and essentially confirms the earlier tabulation of cases of Gorlin, Chaudhry, and Pindborg. The tumor, as previously defined, is made up of odontogenic tissues, with both epithelial and mesenchymal components participating in the proliferation. It is an uncommon tumor, occurring primarily in children and teen-agers, with no obvious predominance of sex or race. Although it occurs in either jaw, there is an apparent predilection for the mandible. On the basis of the extended follow-up in this series, the requirement for additional surgical intervention was significant. The available evidence supported true recurrence in most of these cases, although several probably represented residual tumor with little or no proliferative potential. Cases No. 12 and No. 22 are included in the latter group. The recurrent lesions in these two cases exhibited evident maturational progression toward ameloblastie odontoma and/or odontoma. The relationship between the ameloblastic fibroma and other members of the “mixed” odontogenic tumor has been a matter of discussion in oral pathology circles for some time. There are proponents of the “maturational theory” who believe that the ameloblastic fibroma is the soft-tissue anlage of the odontoma, and that the fibroameloblastic dentinoma and the ameloblastic odontoma (or ameloblastic fibro-odontoma) are intermediate maturational phases. If this theory is true, the whole mixed odontogenic tumor group might be considered to be hamartomatous in nature. Other cases have been reported, such as that by Carr and associates,g in which recurrent lesions, removed months or years later, were again microscopically compatible with ameloblastic fibroma and exhibited no maturational changes. These cases lend credence to the description and classification of the tumor as a neoplastic entity. The truth may be somewhere in between these two poles. Since it is inconceivable that odontomas, fully formed and fully calcified, suddenly appear in the jaw without benefit of a developmental period, a soft-tissue anlage must certainly exist at some stage in its life history. There must, likewise, be intermediate stages between the purely soft-tissue antecedent and the fully calcified dental tissue of the odontoma. Our knowledge of normal tooth development and of the morphologic variations inherent in odontomas assists in the suppositional retracing of odontoma development to recognize that the soft-tissue anlage

Volume Number

33 4

Ameloblastic

fibroma

557

would, indeed, closely resemble the histomorphologic pattern that we recognize as ameloblastic fibroma. On this basis, it would seem apparent that some of the lesions classified as ameloblastic fibromas, in this series and in others, are in reality “soft odontomas.” “ Recurrences” of these lesions are probably merely residual foci, and, if left in situ, these foci may mature further. On the other hand, there seems to be little doubt that a truly neoplastic lesion likewise exists. It would appear to be somewhat more aggressive and to have greater potential for recurrence than is presently appreciated. Unfortunately, the histopathologic features of this neoplasm and the soft-tissue anlage of an odontoma are so similar that, at least at the present time, we are unable to differentiate between the two or to estimate the prognostic probabilities. The problem provides a challenge for future, and more basic, research in the area of the genesis of dental tissues as well as the fundamental nature of certain odontogenic tumors. An additional word of caution in the microscopic evaluation of these tumors must be submitted. We noted earlier in the article that six cases in the initial review were not included because they exhibited histomorphologic changes of the connective-tissue component compatible with a malignant interpretation. (We emphasize that, for the most part, these changes had been recognized by the contributor and/or the AFIP staff at the time of accessioning and were reviewed during this study only as a matter of course.) A study and analysis of these cases will be the subject of a separate article currently under preparati0n.l’ The relevant consideration here is the apparently high ratio of tumors in this general category that may exhibit cellular changes compatible with early or lowgrade malignancy. The significance of the ratios involved and, indeed, of the apparent malignant changes, as well as the natural history of these tumors, is open to question and further examination, In the meantime, however, the careful microscopic review of these lesions is implicit. SUMMARY

A series of twenty-four cases of ameloblastic fibroma of the jaws has been analyzed in order to determine patterns of incidence relative to age, sex, race, site, presenting symptoms, type of treatment, and recurrence. Although the earlier studies of incidence were confirmed, the extended follow-up in this series suggests that the tumor is somewhat more aggressive and has greater potential to recur than is presently appreciated. REFERENCES

1. Thoma, K. H.: The Pathogenesis of the Odontogenic Tumors, ORAL SURG.4: 1262-1280, 1951. 2. Robinson, H. B. G., editor: Proceedings of the Fifth Annual Meeting of the American Academy of Oral Pathology, OELALSURQ.5: 177-178, 1952. 3. Thoma, K. H.: Oral Pathology, a Histological, Roentgenologieal, and Clinical Study of the Diseases of the Teeth, Jaws, and Mouth, ed. 4, St. Louis, 1953, The C. V. Mosby Company, pp. 1213.1235. 4. Bernier, J. L.: Tumors of Odontogenic Apparatus and Jaws, Sec. IV, Fascicle lOa, of Atlas of Tumor Pathology, Washington, D. C., 1960, Armed Forces Institute of Pathology. 5. Shafer, W. Q., Hine, M. K., and Levy, B. M.: A Textbook of Oral Pathology, ed. 2, Philadelphia, 1963, W. B. Saunders Company, pp. 227-234.

558

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1972

6. Pindborg, J. J., and Ck~usen, F.: Clnsaificxtion of Odontogenic Tumors; Suggestion, Acia Odontol. Scnnd. 16: 293-301, 1958. 7. Gorlin, R. J., Chnudhr~-, A. I’., and I’indborg, J. J. : Odontogenic Tumors, Classification, Histopathology and Clinical Behavior in Man and Domestic Animals, Cancer 14: 73-101, 3 961. 8. Small, I. A., and Waldron, C. A. : Xmelol~l:~stomas of t,he Jaws, Oaar, SURG. 8: 281-297, 1955. 9. Cnrr, R. F., Halperin, V., IVood, C., Krust, L., and Schoen, J.: Recurrent Ameloblastic Fibroma, ORAL SURG. 29: 85.90,197O. 10. Leider, A. H., Nelson, ,J. F., and Trodahl, J. N.: Ameloblastic E’ibrosarcoma of the Jaws, ORAL SURO. 33: 559-569, 1972. Reprint requests to : Dr. John N. Trodahl Dental and Oral Pathology Division Armed Forces Institute of Pathology Washington, D. C. 20305