Fibromatous epulis in dogs and peripheral odontogenic fibroma in human beings: Two equivalent lesions David G. Gardner, DDS, h4SD,a and Dale C. Baker, DViU, PhD,b Denver and Fort Collins, Colo. UNIVERSITY OF COLORADO SCHOOL OF DENTISTRY, AND COLLEGE OF VETERINARY MEDICINE AND BIOMEDICAL SCIENCES, COLORADO STATE UNIVERSITY This article compares the clinical and histopathologic features of the peripheral odontogenic fibroma in human beings and the fibromatous epulis in dogs. They are apparently equivalent lesions. Both are odontogenic tumors of limited growth potential that do not recur if adequately excised; both occur in middle and late adulthood of the species concerned. The one difference is that the peripheral odontogenic fibroma is a rare condition, whereas the canine fibromatous epulis is common. (ORAL SURC ORAL MED ORAL PATHOL 1991;71:317-21)

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ome years ago, one of us (D.G.G.), while studying the peripheral odontogenic fibroma in human beings, was shown sectionsof two examplesof canine epulides that appeared to be the counterpart of that lesion, a view that has been expressedrecently by Bostock and White.’ The purpose of the present study is to compare the histopathologic and clinical features of the canine epulis (Fig. 1) with those of the human peripheral odontogenic fibroma. The term jibromatous epulis will be used in this article to refer to canine lesions that have been referred to in the past as either fibromatous or ossifying epulides,* depending on the presenceor absenceof hard tissue such as boneor apparent cementum. They are now considered to be variants of the same lesion.3 MATERIAL

1. Fibromatousepulisin IO-year-old spayed female

AND METHODS

Hematoxylin-and-eosin-stained sections of all 19 casesof canine fibromatous epulides’ accessionedby the Department of Pathology of the College of Vet-

Presentedin part at the Fifth Biennial Congressof the International Association of Oral Pathologists, Tokyo, July 2-5, 1990. aProfessor,Division of Oral Pathology and Oncology, University of Colorado School of Dentistry, Denver. bAssistant Professor, Department of Pathology, College of Veterinary Medicine and Biomedical Sciences,Colorado State University, Fort Collins. 7/14/25580

Fig.

golden retriever.

erinary Medicine of Colorado State University from June 1986 to September 1989 were compared with 18 examples of human peripheral odontogenic fibroma and to casesreported in the literature.4, 5 In addition, attempts were made to obtain further clinical and radiographic information concerning the canine epulides, including follow-up experience. Furthermore, examples of certain other canine conditions that can be confused with fibromatous epulides were *The lesions had usually been accessionedas ossifying epulis or fibromatous (fibrous) epulis. 317

318 Gardner and Baker

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Fig. 2. Fibromatous epulis. Lesion is typically not ulcerated and often exhibits bone or other hard tissues(asterisks) and rests of odontogenic epithelium (E). (Hematoxylineosin stain; original magnification, X6.)

Fig. 3. Fibromatous epulis. Connective tissue component is characteristically very fibroblastic. It often exhibits a pattern in which markedly cellular, densestrands are interwoven with loose areas; however, cellular, dense areas always predominate. (Hematoxylin-eosin stain; original magnification, X 125.)

also studied, including familial gingival hyperplasia in boxer dogs, acanthomatous epulides, and focal hyperplastic lesions of the gingiva. RESULTS

The histopathologic features of the canine fibromatous epulis (Fig. 2) and the peripheral odontogenie fibroma in human beings were similar and consisted of three components. The first was a cellular fibroblastic connective tissue, which was an integral part of the lesion; rather than simply representing stroma, it is essential to the diagnosis of both lesions. In many examples it consisted of markedly cellular, densestrands interwoven with looser areas (Fig. 3). However, this pattern was not always apparent, especially in the fibromatous

Fig. 4. Fibromatous epulis. Photomicrograph is of same tumor shown in Fig. 2 and illustrates rests of odontogenic epithelium located in looser connective tissue. (Hematoxylin-eosin stain; original magnification, X62.5.)

epulides. In these cases the dense connective tissue predominated to the extent that the relatively looser areas were difficult to find. The nuclei of the cells in the densestrands were plump and oval, whereasthose of the less denseareas were spindle shaped. The connective tissue was often highly vascular, with the vessels located in the looser areas. The second component consisted of rests of odontogenic epithelium, the number of which varied (Fig. 4). Consequently, they were not apparent in all sections. The epithelial rests were located in the loose connective tissue. The third component consisted of hard tissue, but again the quantity varied and it was absent in some examples. Some of it was bone (Fig. 5), but somewas of the type considered to be dysplastic dentin in human lesions. This material resembles osteoid but is thought to be a form of dentin only becauseof its close association with odontogenic epithelium. Still other areas of the hard tissue might be interpreted as cementum (Fig. 6). The lesions were covered by mucosal epithelium with a band of lamina propria between the tumor and the epithelium. This submucosal connective tissue often exhibited chronic inflammation. The clinical features of the 19 fibromatous epulides are summarized in Table I. DISCUSSION

Epulides have been known in dogs for a long time. However, the fibromatous epulis of periodontal origin was first described in detail and named by Gorlin et a1.6,’ in 1958 and 1959. It is clear that these workers included in that designation the lesion that is now known as the acanthomatous epuli~.~Moreover, they also considered familial gingival hyperplasia seen in boxers of close ancestry8 as a generalized variant of

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Fig. 5. Bone in fibromatous epulis. This photomicrograph also illustrates numerous blood vessels, which are a common feature of this lesion, and woven pattern of connective tissue. Blood vessels are located in less dense areas. (Hematoxylin-eosin stain; original magnification, X62.5.)

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Fig. 6. Fibromatous epulis exhibiting collagenous material that might be interpreted as cementum. (Hematoxylineosin stain; original magnification, X 125.)

Table

1.Clinical features of 19 fibromatous epulides Feature

the fibromatous epulis. Head,g in the World Health Organization (WHO) classification of tumors of domestic animals, described only one type of epulis, which he termed fibromatous and ossifying epulis. Again, however, his Fig. 26 is that of an acanthomatous epulis. Head also mentions the familial generalized lesion found in boxer dogs. In 1979 Dubielizig et a1.2attempted to standardize the nomenclature of canine periodontal epulides and divided them into three groups: fibromatous epulis, ossifying epulis, and acanthomatous epulis. They pointed out that the acanthomatous epulis had the potential to infiltrate locally into bone, whereas the other two forms were not invasive. The fibromatous and ossifying epulides were separated only on the basis of the presenceor absenceof bone or other calcified material. Barker and Van Dreumeh3 writing in a standard 1985 text, pointed out that there is no prognostic value in distinguishing between the fibromatous and ossifying types, becausethey are all benign tumors that are cured by excision; they therefore referred to them simply as epulides or as epulides of periodontal origin. They distinguished them, however, from the acanthomatous epulis with its invasive properties. Another attempt to reclassify this group of epulides was made in 1987 by Bostock and White.’ They concluded that the fibromatous and ossifying types should be renamed as peripheral odontogenic fibromas becausethey appeared to be the canine counterpart of the human lesion of that name. The latest article on this subject is that of Reichart et al.,‘O who believe that the use of the term peripheral odontogenicjibroma adds to the “nomenclatural chaos.” They consider the lesions that have been termed fibromatous and ossifying epulides to be

Breeds represented (n = 15) Boxers Golden retriever Other Jaw (n= 11) Maxilla Mandible Region (n = 13) Incisor/cuspid Maxilla Mandible NS Premolar Maxilla Mandible NS

Molar Age W (n = 19) Mean Range Sex (n = 19) M F Lesion size (cm) (n = 10) 0.5-1s 3x2

11 breeds 3 dogs 3 dogs 9 dogs (one of each) 9 4

6

4

0

2 0 8.3 4.9- 14.5 8 11 9 1

Two cases were referred because of recurrence. None recurred after excision. iyS. Not specified.

inflammatory hyperplastic lesions, with or without metaplastic bone formation. The peripheral odontogenic fibroma in human beings was first illustrated in a WHO publication in 1971.I’ However, at the time, another unrelated lesion, now generally known as the peripheral ossifying fibroma, was also being referred to as a peripheral odontogenic fibroma. Consequently, Gardner,5 in an attempt to distinguish between the two different lesions with the same name, referred to the lesion il-

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Fig. 7. Acanthomatous epulis. This lesion consists of sheets of squamous epithelium within connective tissue stroma. Basal cells are often unremarkable but some, as in this example, exhibit vacuolization and polarization of nuclei away from basement membrane. (Hematoxylin-eosin stain; original magnification, X 125.)

lustrated in the WHO publication as the peripheral odontogenic fibroma (WHO type). The WHO designation is no longer necessary,’2 provided the term peripheral odontogenic jbroma is not used for the peripheral ossifying fibroma; consequently it will not be used in this article. The word peripheral, when applied to odontogenic tumors, refers to a lesion occurring solely in the soft tissues covering the toothbearing parts of the jaws (i.e., the gingiva and alveolar mucosa). The peripheral odontogenic fibroma is an elevated, nonencapsulated lesion of the gingiva and alveolar mucosa. It is rare, with only 41 reported cases.12 However, even some of these may not in fact represent that lesion, at least as originally described. For instance, Buchner et al. I3 believed that its histologic spectrum was wider than had been originally described and included examples that exhibited loose connective tissue, markedly cellular fibroblastic connective tissue, or dense connective tissue. They included examples such as their case 7, which appears to be a peripheral ameloblastoma, and others with mature connective tissue componentsthat other workers probably would not have accepted as peripheral odontogenic fibroma. Similarly, some of the casesin the report of Kennedy et a1.i2appear to represent focal fibrous hyperplasia with odontogenic rests rather than peripheral odontogenic fibroma. The tumor with which the canine fibromatous epulis is being compared in this article, in contrast to focal fibrous hyperplasia, exhibits the classic fibroblastic appearance first illustrated by Pindborg et al.” and described in detail by Farman and by Gardner.5 Given the rarity of the lesion, it is not feasible to make firm

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conclusions, but on the basis of the literature, the peripheral odontogenic fibroma appears to occur over a wide age range, in either jaw, and about equally in both sexes.Only one casehas beenreported to recur.12 The basic conclusion from this study, in agreement with that of Bostock and White,’ is that the fibromatous epulis of dogs is the canine equivalent of the human peripheral odontogenic fibroma. The histopathologic appearanceof the two lesions is identical. A second conclusion is that, as Barker and Van Dreume13 point out, there is no point in distinguishing between fibromatous and ossifying epulides; they are part of the same histopathologic spectrum and there is no prognostic significance in separating them. It would be preferable if the terms in veterinary and human pathology coincided and that peripheral odontogenic fibroma were usedas standard terminology. However, realistically, the term jibromatous epulis is so entrenched in veterinary medicine that it will probably continue to be used. Whereas the human peripheral odontogenic fibroma and the canine fibromatous epulis are identical histologically, there is a significant difference in the prevalence in the two species.The canine lesion is the most common oral neoplasm in dogs, whereas the human peripheral odontogenic fibroma is very rare. In human beings there is an intraosseous counterpart to the peripheral odontogenic fibroma, but we are unaware of an intraosseous counterpart of the fibromatous epulis in dogs. The human peripheral odontogenic fibroma does not tend to recur after adequate excision, whereas a difference of opinion concernsthe biologic behavior of the canine lesions. Barker and Van Dreume13state that they are cured by excision. On the other hand, Bostock and White’ reported three recurrences in 17 casesof the canine lesion, and Bjorling et a1.i4recommended that all epulides be treated similarly because they claim that all three types of epulides (fibromatous, ossifying, and acanthomatous) tend to recur after inadequate excision. There are two points to consider in this connection. First, any lesion may recur if inadequately excised. It follows that when the preoperative diagnosis has been confirmed by biopsy as fibromatous epulis, surgeons should make sure that their excision is down to bone and that all remnants of tumor are thoroughly removed from between the teeth and from their lingual aspects,rather than superficially excising the lesion from the buccal aspect. A useful precaution in an attempt to avoid recurrence would be to cauterize the wound. It should not be necessary,however, as Bjorling et al. l4 have recommended,to perform an en bloc resection of bone and teeth or to extract the associated

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teeth. In any event, recurrence of a benign growth of the gingiva should not be considered an important surgical failure; the lesion can always be reexcised if necessary. A second reason that fibromatous epulides are thought by someto tend to recur is that sufficient emphasis had not been placed in the past on the difference between the biologic behavior of these lesions and that of the acanthomatous epulis. Unlike the fibromatous epulis, the acanthomatous epulis infiltrates bone and characteristically tends to recur.2 There are three lesions occurring in dogs with which the fibromatous epulis may be confused histologically. The first is the acanthomatous epulis,2 but its histopathologic appearance is different (Fig. 7), consisting of sheets of squamous epithelium that infiltrate connective tissue and trabecular bone. The connective tissue may be cellular and thus similar to that of the fibromatous epulis, or it may be relatively acellular, dense connective tissue. Moreover, hard tissue may be present, as in the fibromatous epulis. The differential diagnosis is based primarily on the characteristic epithelial proliferation of the acanthomatous epulis, not on the stromal component. The secondlesion is a focal growth of hyperplastic connective tissue. It is a reaction to irritation, such as dental calculus or plaque, and is very common in human beings, where it is referred to by a number of terms. It is often called an irritation fibroma, although this is inaccurate becauseit is not a true neoplasm. It is also called a fibroid epulis, which adds to the confusion in this discussion becauseit is different from the peripheral odontogenic fibroma and the fibromatous epulis. An alternative term is focal fibrous hyperplasia, which would also be an acceptable term in veterinary medicine, to distinguish it clearly from the fibromatous epulis. This reactive lesion consists of relatively acellular connective tissue, not the cellular, fibroblastic type of the fibromatous epulis, and may exhibit metaplastic bone. The third lesion with which the fibromatous epulis may be confused is familial gingival hyperplasia seen in boxer dogs of close ancestry.8 According to Brodey,” it occurs to some extent in about 30% of boxers more than 5 years old. Microscopically, the lesion consists of proliferation of fibrous connective tissue in which osseousfoci may be seen. It does not exhibit the fibroblastic connective tissue seen in fibromatous epulides. Both the canine fibromatous epulis and the peripheral odontogenic fibroma in human beings should be considered neoplasms with limited growth potential. Reichart et aLlo believe the fibromatous epulis to be reactive, but its histologic appearance is not that of a

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reactive lesion, in which an inflammatory component would be expected to be prominent. The present series is too small to draw significant conclusions about the clinical features of fibromatous epulis. However, the lack of examples in the molar region is noteworthy. Moreover, it is apparent that the lesion occurs primarily in dogs more than 5 years old. Some authors state that the fibromatous epulis is more common in boxer dogs than in other breeds,16 whereas others disagree.7Again, the present series is too small to settle the issue. The idea that these epulides have a predilection for boxers may be caused by confusing them with the diffuse gingival hyperplasia that occurs in boxers of close ancestry.8

REFERENCES

1. Bostock DE, White RAS. Classification and behaviour after surgery of canine “epulides.” J Comp Path011987;97:197-206. 2. Dubielzie RR. Goldschmidt MH. Brodev RS. The nomenclatureof p&ddntal epulides in dogs. Vet Path011979;6:209-14. 3. Barker IK, Van Dreumel AA. The alimentary system. In: Jubb KVF, Kennedy PC, Palmer N, eds. Pathology of domestic animals; vol 2. 3rd ed. New York: Academic Press, 1985:17-9. 4. Farman AG. The peripheral odontogenic fibroma. ORAL SURG ORAL MED ORAL PATHOL 1975;40:82-92. 5. Gardner DG. The peripheral odontogenic fibroma: an attempt at clarification. ORAL SURG ORAL MED ORAL PATHOL 1982; 54:40-8. 6. Gorlin RJ, Clark JJ, Chaudhry AP. The oral pathology of domesticated animals. ORAL SURG ORAL MED ORAL PATHOL

1958;11:500-35. 7. Gorlin RJ, Barron CN, Chaudhry AP, Clark JJ. The oral and

pharyngeal pathology of domestic animals: a study of 487 cases.Am J Vet Res 1959;20:1032-61. 8. Burstone MS, Bond E, Litt R. Familial gingival hypertrophy in the dog (boxer breed). Arch Path01 1952;54:208-12. 9. Head KW. Tumours of the upper alimentary tract. Bull WORLD Health Organ 1976;53:145-67. 10. Reichart PA, Phillipsen HP, Durr U-M. Epulides in dogs. J Oral Path01 Med 1989;18:92-6. 11. Pindborg JJ, Kramer IRM, Torloni H. Histological typing of odontogenic tumours, jaw cysts and allied lesions. International histological classification of tumours No. 5. Geneva: World Health Organization, 1971:30-l. 12. Kennedy JN, Kaugars GE, Abbey LM. Comparison between the peripheral ossifiying fibroma and peripheral odontogenic fibroma. J Oral Maxillofac Surg 1989;47:378-82. 13. Buchner A, Ficarra G, Hansen LS. Peripheral odontogenic fibroma. ORAL SURG ORAL MED ORAL PATHOL 1987;64:432-8. 14. Bjorling DE, Chambers JN, Mahaffey EA. Surgical treatment of enulides in dogs: 25 cases(1974-1984). J Am Vet Med Assot -1987;190:13i5-8. . 15. Brodey RS. A clinical and pathologic study of 130 neoplasms of the mouth and pharynx of the dog. Am J Vet Res 1960; 21:787-812. 16. Howard EB, Nielson SW. Neoplasia of the boxer dog. Am J Vet Res 1965;26:1121-31. Reprint requests to:

David G. Gardner, DDS, MSD University of Colorado School of Dentistry 4200 E. Ninth Ave., Box C284 Denver, CO 80262

Fibromatous epulis in dogs and peripheral odontogenic fibroma in human beings: two equivalent lesions.

This article compares the clinical and histopathologic features of the peripheral odontogenic fibroma in human beings and the fibromatous epulis in do...
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