The histopathologic findings in 583 cases of epulis fissuratum Duane E. Cutright, UNITED
STATES
WALTER
REED
ARMY ARMY
Colonel, DC, USA* INSTITUTE MEDICAL
OF DENTAL CENTER,
RESEARCH,
WASHINGTON,
D. C.
The histopathologic findings in 583 cases of epulis fissuratum discussed. The clinical data, such as age, sex, etc., are tabulated. pathologic entities are identified within the fibrous connective fissuratum tumors. The significance of these findings to the pathologist is discussed.
are presented and Seventeen different tissue of epulis prosthodontist and
E
pubs fissuratum (EF) typically occurs around the borders or flanges of full or partial dentures in either the maxilla or the mandible. It is most often described as being a raised, sessile or pedunculated lesion, composed of dense fibrous connective tissue, resulting from the constant trauma and inflammation caused by the pressure of the denture flange. There have been many reports which contained data on the clinical appearance, etiology, incidence, and treatment of epulis fissuratum.l, * The largest, and one of the best, of the recent reports was that of Nordenram and Landt.3 They reported that most cases occurred in persons between 50 and 60 years of age (37.7 per cent), with a high incidence in women (81.2 per cent) and equal frequency of occurrence between the maxilla and the mandible. However, I have found no report giving the histopathologic changes occurring within these tumors. This report comprises the histologic and clinical findings from 583 cases on file at the United States Army Institute of Dental Research. Only 576 records were available for study, and many of them were deficient with respect to certain of the data surveyed. Therefore, many of the figures given will not equal 100 per cent of the 583 cases. An attempt was made to delineate the histologic findings in the epithelium, *Chief, Division
of
Oral Pathology. 401
402
Cutright
Table
I. Location
Oral Surg. March, 1974
116 164 19 20 13 15 8
Mandible Maxilla Lower anterior teeth Floor of mouth Molar area Premolar area Hard palate
Table
Sex
teeth
Whites Negroes Males Females
520
Based on 535 records listing
race
1;; 358
Based on 555 records listing
sex
Ill. Age at occurrence
Age
Number
2 7 65 72 124
l-9
10-19 20-29 30-39 40-49
Table
175 38 36 25 5 1
II. Race and sex Race
Table
Buccal side Lingual side Upper anterior Cuspid area Incisor area Soft palate
IV. Duration Duration 1-4 wks. l-6 mos. 7-12 mos. 1-25 yrs.
Age
Number
50-59 60-69 70-79 80-89
129 96 36 7
Duration
Number
of lesion Number if 14 13
2-3 yrs. 3-4 yrs. 4-5 vrs. 6, 7,“8, and 10 yrs.
2 3 5 1 each year
propria, and submucosa. Any changes concerning blood vessels, salivary glands, and nerves were also noted. In addition, clinical data concerning age, sex, race, occupation, location, and duration were compiled.
lamina
FINDINGS Clinical
The clinical appearance of the lesion was variable and ran the gamut from red, easily bleeding lesions, such as pyogenic granuloma, to those lesions described as pale, firm, and composed of dense fibrous connective tissue, such as an irritation fibroma. The morphology was described as raised, sessile,or pedunculated. Ulceration wa.sreported to have been present in fifty-one cases. Most cases (116) occurred in the anterior maxilla. Also, more casesoccurred on the buccal (175) than on the lingual (38) side. A summary of the findings pertaining to location is given in Table I. With respect to sex incidence, the study showed 197 males to 355 females affected, or 36 per cent males as compared to 64 per cent females. hyperemic,
Volume Number
Table
Epdis
37 3
V. Epithelial
403
changes No.
Change Acanthosis Hyperparakeratosis Marked acanthosis resembling pseudoepitheliomatous Ulceration Hyperkeratosis Inflammatory papillary hyperplasia Vesiculation Spongiosis Odontogenic type of epithelium Dyskcratosis (benign) Keratin cyst
Table
fisuratum
of cases
Almost Almost
100% 100% 222 57 41 31 19 18 18 10 1
hyperplasia
VI. Connective tissue changes Change
Focal odontodysplasia Osseous metaplasia Chondromatous metaplasia Nodular lymphoid hyperplasia Microabscesses Increased numbers of eosinophils Ectopic sebaceous glands Foreign-body giant-cell reaction Bone or dentin sequestra Traumatic neuroma Amalgam tattoo Sebaceous cyst
No.
of cases 48 29 25 15 8 8 7 3 2 1 1’
The racial breakdown was 520 Caucasians to 15 Negroes, or 97 per cent Caucasian and 3 per cent Negro (Table II). The age distribution was from 6 to 89 years, with the fifth and sixth decades having 48 per cent of the total (Table III). The duration (Table IV) as determined from the histories varied from 1 week to 10 years, with 40 per cent of the patients reporting that the lesion was present from 6 months to 2 years. There were twenty-two different occupations listed, with housewives accounting for 35 per cent; active military personnel, 24 per cent; retired personnel, 8 per cent; oft-lee workers, 5 per cent; and sales personnel, 4 per cent. When a correlation was attempted between epulis fissuratum and associated pathosis in other organs, thirty different pathologic conditions were listed on the records. Despite this large number, there were never more than five patients with any one type of associated pathologic condition. Histopathology
Epithelial changes. The many epithelial changes found are listed in Table V. Most of these changes were in the tissue directly traumatized by the denture flange. Spongiosis was present in eighteen cases, and an unusual homogeneous eosinophilic vesiculation was present in nineteen cases(Fig. 1). Severe acanthosis resembling pseudoepitheliomatous hyperplasia was present in 222 casesbeneath the flange area of the denture.
Oral March,
Fig. 2. Section of acanthotic epithelium showing Fig. 2’. Section through base of epulis fissuratum the flange had impinged upon the tissues. The bottoms reaction.
Burg. 1974
vesieulation and hyperparakeratosis. tumors. Three clefts are shown where of the clefts show a dense inflammatory
Connective tissue. Table VI contains a summary of the changes found within the connective tissue. In some slides as many as five different grooves could be seen where the denture had at one time or another impinged on the tissue. With few exceptions,
Volume 37 Number 3
Fig. PI. Section showing focal odontodysplasia. Fig. 4. Section of connective tissue showing sebaceous cyst (upper).
Epulis
sebaceous gland
fissuratum
(bottom)
405
and associated
the inflammation was most prominent directly beneath the denture flange (Fig. 2). In addition to the osseousand chondromatous metaplasia (reported elsewhere), there were forty-eight casesof focal odontodysplasia (Fig. 3). One of the ectopic sebaceous glands appeared to be forming a sebaceous cyst (Fig. 4). Two areas resembling small hemangiomas and one focal area resembling a lymphangioma were noted. In areas where the denture had directly traumatized muscle, the muscle bundles had been infiltrated by eosinophil$. Occasionally these bundles had been completely replaced by eosinophils and cells of the inflammatory type (Fig. 5). Fifteen casesof a nodular type of lymphoid hyperplasia were found (Fig. 6). Periductal fibrosis was present occasionally, and one case showed marked scarring around the duct. Sequestra of bone or dentin were found in two cases. Blood vessel changes. Changes in the walls of the blood vesselswere difficult to assess.It was virtually impossible to decide what represented normality, especially on the palate and over the alveolar processes. However, I compiled a list of 145 cases in which some hyperplastic or sclerotic change in the vessel wall was found. This could involve any one or all three layers of the vessel wall (Fig. 7). Several cases showed sclerosis plus a fibrinoid change reminiscent of polyarteritis nodosa. Fibrosis of the adventitia occurred around both arteries and veins. A recanalized thrombus was found in one case. Perineural fibrosis was an uncommon finding in association with the perivascular fibrosis and sclerotic changes of the vessels. Minor salivary glands. Minor salivary glands were present in 251 of the cases
Oral March,
Fig. 5, A, Section eosinophils
and
through
area
of
traumatized
muscle.
B,
High-power
view
Burg. 1974
showing
histiocytes.
studied. Table VII shows the histopathologic findings within these glands. In many of the cases showing increased collagenization, only the ductal epithelium remained as evidence of a pre-existing salivary gland (Fig. 8). DISCUSSION The finding of the largest numbers of EF tumors in the upper and lower anterior areas corresponds to the clinical experience of the prosthodontists and agrees with Nordenram and Landt.3 The anterior maxilla showed twice as many tumors as the anterior mandibular area. Nordenram and Landt found approximately equal numbers in both arches. All of the areas covered by dentures are susceptible to the formation of EF, as shown by the finding of eight caseson the palate, twenty in the floor of the mouth, and thirteen in the molar area. Approximately four times as many caseswere found to the buccal of the ridge as to the lingual. These findings are also in agreement with the findings of
Volume Number
Fig * 6. Section th rough beneath the epithelium. Note
Table
Epulis
37 3
epithelium the nodular
and lamina accumulations.
propria.
A
dense
fissuratum
infiltrate
407
is pr .esent
VII. Histopatl nologic findings
Sialadochitis Sialadenitis Mucous metaplasia of ductal epithelium Ductal ectasia (marked) Squamous metaplasia of ductal epithelium Ductal epithelial hyperplasia Abscesses Lymphoid hyperplasia
Most
cases 215 16 :; 4 2 1
Nordenram and Landt. This was expected because it is difficult to tip a lower denture to the lingual and the upper denture has no lingual flange. The finding that 65 per cent of the cases were in female patients is surprising because, since this is a military facility, we are usually male biased in our studies. However, Nordenram and Landt also found that 81.2 per cent of their cases occurred in female patients. This is possibly due to the fact that female patients wear their dentures more often and perhaps for longer periods of time for esthetic purposes. However, this would not appear to be a complete answer. Epulis fissuratum can be found in any age group, even in infants. In this study the youngest patient was 6 and the oldest was 89 years of age. This clearly shows that the defensive reaction of the primitive mesenchymal tissue is retained throughout the individual’s life. As was expected, most of the cases occurred during the fifth and sixth decades, which compared to the sixth and seventh decades reported by Nordenram and Landt.3 In the findings 35 per cent of the cases were represented by housewives and
408
Fig
Cutright
Oral March,
Surg. 1974
Fig.
7
(a)
Fig. and Fig.
7. Section of deep connective tissue. Note the decrease in size of the vascular the increased thickness of the walls (b). 8. Section in deep connective tissue. Note preservation of ductal cells.
lumen
24 per cent by active duty personnel. It is difficult to explain or to ascribe any significance to this predominance of housewives. The chronicity and lack of symptoms in many cases of epulis fissuratum were substantiated by our findings that these lesions were stated to have been present as long as 10 years. Forty per cent of the cases were present from 6 months to 2 years. There was no correlation in this study between epulis fissuratum and other distant pathologic conditions. This would indirectly indicate there is little relation between the loss of teeth and pathologic conditions elsewhere in the body. In both arches, however, the papillary enlargements of inflammatory papillary hyperplasia were occasionally found. Acanthosis and hyperparakeratosis were present in nearly every case of El?. These were the first histologic manifestations of the body to trauma and irritation and represent the initial defensive reaction of the epithelium. The hyperparakeratosis occurred under the very edge of the flange if the trauma was not too severe and at the margins of the flange area when the trauma was very severe. This was especially true when there was ulceration present beneath the flange. The thickening and widening of the rete pegs were also evidenced in the surrounding area of relatively normal tissue removed by the surgeon at the base of the lesion. In these cases it appeared to result from the minor trauma of denture wearing. Another defensive reaction manifested by extreme lengthening of the rete pegs was the pseudoepithelioma-like hyperplasia found at various
8
Epu1i.s fissuratum
409
points where the chronic inflammation was prominent. Both acanthosis and pseudoepithelioma-like hyperplasia contributed to the lengthening of the rete pegs. Although ten cases of dyskeratosis were found, these changes occurred in association with ulceration, intense inflammation, or under the denture flange. This, therefore, must be considered only as benign dyskeratosis. No evidence of any malignant change was found. The peculiar eosinophilic vesiculation found in the very upper layers of the stratum spinosum and even in the parakeratinized layers occurred only above areas showing inflammation, hyperemia, and dilated capillaries. These vesiculated areas gave the appearance of being filled with a filtrate from the vessels. This is probably the same material discussed by Archard and G1ass.4 They found it to be rich in protein, carbohydrate, tryptophan, and sulfhydryl groups. The effect of this fluid on bacterial growth and, therefore, indirectly on the inflammatory reaction is speculative. In ten cases the epithelium was thinned and not acanthotic. This reaction was seen most often where there had been large amounts of collagen deposited within the tumor, which then resembled an irritation fibroma. The findings in the lamina propria were mostly the result of injury and repair. Indeed, all stages of inflammation and repair were found, often in a single slide. This disagrees with Chang,5 who states that the early highly vascular lesions resembling pyogenic granuloma are found in pregnant women and that the dense fibrous type is manifested only as a result of chronic irritation. These cases were most commonly found around the area of impingement by the denture flange. The cases of osseous and chondromatous metaplasia are discussed elsewhere.6 The amalgam tattoo, ectopic sebaceous glands, microabscesses, hemangiomas, dilated lymph vessels, and traumatic neuroma were interesting and incidental findings and represent pathosis which appears in these areas when the patient does not wear dentures. However, it is pointed out that the pathologist and the surgeon must be aware of the interrelationship of these conditions within the tumors of EF to avoid a wrong diagnosis or treatment. The cases listed as focal odontodysplasia may in part represent small tooth fragments left from previous surgical procedures. However, most of these were partially to completely circumscribed by peculiar cuboidal epithelioid cells of undetermined origin. Similar calcification without the encircling epithelioid cells is commonly found in biopsy material from the oral areas. The deeper connective tissue, like the lamina propria, showed all types of inflammation and various stages of repair. Peculiar in this deeper tissue was the degeneration and sometimes the disappearance of muscle fibers where the trauma had been more severe. Often associated with this degeneration was the appearance of an inflammatory reaction particularly high in eosinophils. This resembles the traumatic granuloma described by Bhaskar and Lilly,’ where the muscles of the tongue were traumatized. Fifteen cases of nodular lymphoid structures were found. These were often associated with a minor salivary gland duct. Histologically, the nodules appeared normal and no reason for their formation was evident. Periductal fibrosis and sequestra of bone or tooth fragments were present in two cases. Again, these findings are not uncommon in the oral cavity where the mouth has been prepared for full dentures.
410
Cutright
Oral March,
Burg. 1974
The large number of cases (145) of sclerotic changes within the blood vessels could not all be attributed to previous surgery. Many of these changes were away from the area where surgical procedures are typically performed. This was especially true when they occurred on the palatal area. Certain of these changes were reminiscent of glomera but most likely represented perivascular fibrosis. However, special stains were not employed. The impact of this much vessel sclerosis could possibly have a physiologic effect on the denture-bearing areas by decreasing the blood supply and lymph drainage. Whether or not it could be directly related to denture stress is highly probable but not proven. Not surprisingly, minor salivary glands were found in 251 cases; of these, 215 showed some evidence of sialadenitis. These glands showed the effect of denture trauma by the following manifestations: In the ducts mucous metaplasia and squamous metaplasia were common, and ectasia and hyperplasia were also found. Acinar atrophy occurred quite commonly, and at times was so severe that only the ducts remained to indicate that a minor gland had ever been present. The ducts were markedly more resistant and remained amazingly normal in appearance despite the disappearance of the acinar cells. One case looked very much like adenocystic carcinoma. The additional pathosis in the salivary glands included other types of metaplastic reactions and lymphoid hyperplasia. SUMMARY
The complete gamut of pathologic changes which occurred in the tissue removed and diagnosed as epulis fissuratum has been presented. An unusually large number of separate pathologic entities was found associated with EF. Most of them can be attributed to denture trauma and inflammation and healing affecting the normal tissues present. The clinical manifestations and the histopathologic findings have been presented. The following unusual or new findings have been discussed incident to this report : (1) EF can manifest itself clinically and histologically as granulation tissue (that is, pyogenic granuloma) or as dense fibrous connective tissue (that is, irritation fibroma) , or any combination of these. It, therefore, represents injury-healing-reinjury, etc. (2) It is most often asymptomatic. (3) It is found more often in the maxilla than in the mandible. (4) It is found most often in the anterior areas of both jaws. (5) It is found most often under the buccal or labial flange, (6) It occurs predominantly in females. (7) It occurs from childhood to very old age, most often in the fifth and sixth decades. (8) It may be present for weeks to years. (9) According to occupation, housewives were most often affected. (10) There was no correlation with any other disease. (11) Acanthosis and hyperparakeratosis were present in virtually 100 per cent of the cases. (12) Inflammatory papillary hyperplasia occurred in association with EF. (13) The following pathoses were found within the tissue biopsied as EF: microabscesses, areas of focal odontodysplasia, osseous and chondromatous metaplasia, traumatic neuroma, muscle degeneration, amalgam tattoo, sebaceous glands, sebaceous cyst, hemangiomas, lymphangioma, nodular lymphoid accumulations, sialadenitis, and several types of ductal metaplasia and vascular sclerosis.
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Epu1i.s fissuratum
411
RERRENCES
Lantzman, E.: Conservative Treatment of Large Hyperplasia of the Oral Mucosa Caused by Denture Irritation: Report of a Case, ORAL ~TJRQ. 26: 626-629, 1968. Arwill, T., Nilsson, B., and Ober cf.: Eve&on of Columnar Epithelium in Denture-Induced Hyperplasia of the Oral Mucous fi embrane of Man, Arch. Oral Biol. 13: 589-591, 1968. Nordenram, A., and Landt, Ho&: Hyperplasia of the Oral Tissues in Denture Cases, Acta Odontol. Scand. 27: 481-491, 1969. Archard, H. O., and Glass, N. M.: Degenerative Changes in the Superficial Epithelium of Chronic Hyperplastic Oral Mucosa: Clincopathological and Histochemical Study, J. Dent. Res. 49: 1118-1124, 1970. 5. Chang, P. : A Clinical Statistical Study of Epulis Patients, Odontology (Tokyo) 58: 212221, 1970. 6. Cutright, D. E.: Osseous and Chondromatous Metaplasia Caused by Dentures, ORAL SURG. 34: 625-633, 1972. 7. Bhaskar, 8. N., and Lilly, G. E.: Traumatic Granuloma of the Tongue (Human and Experimental), ORAL Suao. 18: 206-218, 1964. Beprint requests to: Colonel Duane E. Cutright Division of Oral Pathology U. 8. Army Institute of Dental Research Walter Reed Army Medical Center Washington, D. C. 20012