J. Nihon Univ Sch. Dent., Vol. 33, 166-173, 1991

Pathological Study of the Hyperplastic Dental Follicle

Yohko FUKUTA 1, Morio TOTSUKA 1, Yasunori TAKEDA 2 and Hirotsugu YAMAMOTO 3

(Received 22 February and accepted 9 April 1991)

Key words: dental follicle, hyperplasia, odontogenic fibroma, impacted Abstract Eleven specimens of hyperplastic dental follicles were studied clinicopath- ologically, with reference to the patient's sex and age at the time of diagnosis, site of the lesions, and histopathology. The patients comprised 6 males and 5 females with an average age of 15.7 years (range 10 to 23 years). Two cases involved multiple lesions, and 9 a single lesion. The lesions were related to impaction of the canine, second , second or third molar. Radiographically, the lesions showed various degrees of radiolucency around the crown of the impacted tooth. Most of the cases were diagnosed clinically as . The histopathological features of the lesions were similar to those of normal dental follicular tissue around the developing tooth. No tumorous features such as odontogenic fibroma, odontogenic myxoma or myxofibroma were evident in the lesions. Introduction Hyperplastic dental follicle around an embedded tooth is an asymptomatic lesion occasionally showing slight swelling in the affected area. It appears radio- graphically as a well circumscribed cystic radiolucency surrounding the crown of the impacted tooth and has often been misdiagnosed clinically as dentigerous cyst. Histologically, such hyperplastic dental follicles are composed of a mass of densely or loosely arranged connective tissue containing scattered odontogenic epithelial rests, and such findings have been confused with odontogenic fibroma, odontogenic myxoma, odontogenic myxofibroma or other odontogenic tumors. GARDNER [1]described three different lesions which had been reported as central odontogenic fibromas, i. e., hyperplastic dental follicle, simple central odontgenic fibroma, and central odontogenic fibroma (WHO type). The first type is now not generally regarded as a tumorous condition, but there have been few detailed studies of hyperplastic dental follicles. Therefore, the purpose of the present study was to examine the histopathological features of hyperplastic dental follicles in

1 福 田容 子,戸 塚 盛雄: Department of Oral Diagnosis, School of , Iwate Medical University 2 武 田泰 典: Department of Oral Pathology, School of Dentistry, Iwate Medical University 3 山本 浩 嗣: Department of Oral Pathology, Nihon University School of Dentistry at Matsudo. To whom all correspondence should be addressed: Dr. Yohko F UKUTA,Department of Oral Diagnosis, School of Dentistry, Iwate Medical University, 1-3-27 Chuo-dori, Morioka 020, JAPAN. 167 order to differentiate them from some types of odontogenic fibroma, and to discuss the causes of these lesions around impacted teeth. Materials and Methods Eleven cases were obtained from the files of the Department of Oral Pathol- ogy, School of Dentistry, Iwate Medical University, covering the past 10 years. Patient age and sex, lesion site, radiographic findings, and clinical diagnosis at the first examination were recorded in each case. Surgically resected specimens which had been fixed in 10% neutral buffered formalin and embedded in paraffin were sectioned at a thickness of 5 p.m and prepared for hematoxylin and eosin staining. The stained sections were examined histopathologically with particular reference to odontogenic epithelium, calcified materials, and features of fibrous connective tissue. Results Clinical findings (Table 1) Patient age and sex The patients in the present cases had an average age of 15.7 years with a range of 10 to 23 years.

Table 1 Clinical data on cases of hyperplastic dental follicle

There was no predominant sex predilection; 6 of the patients were males and 5 were females. The two patients presenting with multiple lesions were a 14-year- old male (4 lesions) and an 18-year-old male (2 lesions). Lesion site Of the 15 lesions in 11 cases, 8 lesions occurred in the and 7 in the . The sites of the lesions were as follows: 4 in the canine, 2 in the second premolar, 5 in the second molar, and 4 in the third molar. Two cases involved multiple lesions: bilateral upper and lower second molars in case 8 and bilateral upper third molars in case 11. Clinical features Most of the patients had no clinical symptoms at the site of the lesions, except 168 for slight swelling in a few cases. In only one case (case 4), there was spontaneous pain due to infection. In most of the cases involving a single lesion, the tooth opposite the impacted one had already erupted. Case 8 involved multiple symmet- rical lesions, but the patient had no significant past or family history. Radiographic findings The crown of the impacted tooth was surrounded by a well demarcated radiolucent lesion with a thin layer of peripheral radiopacity (Fig. 1). A few, small tooth-like radiopacities were seen around the lesions in cases 9 and 11. In two cases (cases 3 and 7), slight resorption of the root of the neighboring proximal tooth was revealed. Clinical diagnosis The clinical diagnoses were as follows: dentigerous cyst in 9 lesions of 6 cases, in 3 lesions of 2 cases, ameloblastoma in 1 case, in 1 case, and embedded tooth in 1 case. Histopathological findings The hyperplastic dental follicle was composed of relatively delicate and mature collagen fibers (Fig. 2) associated with partial myxomatous change, which showed various amounts of ground substance stained with hematoxylin. The border of the hyperplastic dental follicle was clear, and occasionally covered with thin alveolar bone. All of the lesions contained several to numerous epithelial components, except for one case (case 2). Epithelial components of the hyperplastic dental follicles in the present study were classified into the following three types: reduced enamel epithelium (REE), ribbon-like arrangement of the remnant of the dental lamina (RDL), and scattered odontogenic epithelial rest (OER) in fibrous connec- tive tissue. REE was found in eight lesions. Most of the epithelial cells in REE were columnar to cuboidal in shape, and had pyknotic nuclei and eosinophilic cytoplasm (Fig. 3). Occasionally, these epithelia had undergone squamous cell metaplasia (Fig. 4), or bud-like proliferation (Fig. 3). Ribbon-like arrangement of the RDL (Fig. 5) was seen in three lesions. The cells of the RDL were smaller in size than those in REE, round in shape, and had small round nuclei and pale cytoplasm. The nest of the RDL formed strands and often displayed keratiniza- tion. Scattered, double-stranded OER (Fig. 6) in fibrous connective tissue was observed in 10 lesions. Vacuolar degeneration and keratinization were sometimes seen in the scattered OER. Small or cementicle-like calcifications were found in eight lesions. The type of calcification was classified into the following four patterns: calcification near REE, calcification around OER, calcification in OER, and calcification scattered in fibrous connective tissue. Calcification near REE was seen in three lesions, two of which showed numerous cementicle-like calcifications (Fig. 7). In case 1, calcification was often seen around OER (Fig. 8). In case 11, calcification was found in OER which displayed squamous cell metaplasia and formation of microcysts (Fig. 9). Small tooth-like radiopacities recognized in X-ray photographs in cases 9 and 11 were diagnosed as supernumerary teeth (microdonts) by microscopic examina- tion. 169

1

2

3

Fig. 1 Radiograph of case 11. A well defined, cystic radiolucency can be seen surrounding the crown of the impacted right maxillary third molar. An impacted supernumerary tooth is also present. Fig. 2 Microscopic view of the whole cut surface of the hyperplastic dental follicle (Case 10).(H. E. stain. •~ 5.7) Fig. 3 Microscopic view of the reduced enamel epithelium. Pyknotic nuclei and eosinophilic cytoplasm of the inner enamel epithelium, and bud-like proliferation of the outer enamel epithelium are evident. (H. E. stain. •~ 229) 170

4

5

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Fig. 4 Squamous cell metaplasia of the reduced enamel epithelium (H. E. stain . •~ 75) Fig. 5 Ribbon-like arrangement of a dental lamina remnant (H. E. stain . •~ 114) Fig. 6 Scattered, double-stranded odontogenic epithelial rest in fibrous connective tissue (H. E . stain. •~ 114) 171

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8

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Fig. 7 Reduced enamel epithelium asssociated with small calcified globules (H. E. stain. •~ 75) Fig. 8 Cuffing calcification of odontogenic epithelial rests (H. E. stain. •~ 150) Fig. 9 Calcification and formation of microcysts within an epithelial nest with squamous cell meta- plasia (H. E. stain. •~ 114) 172

Discussion Several reasons for retarded eruption or impaction of teeth have been de- scribed. These include general causes (endocrine disturbance, vitamin deficiency or genetic factors) and local causes (lack of eruptive space, ankylosis, supernumerary teeth, development of tumor or cysts, malposition, insufficient growth and eruptive force or localized growth disturbance of the jaws)12'31. The upper and lower canines, second and third molars frequently become impacted because of a lack of space resulting from the anatomical shape of the jaws, premature loss of , or chronological order of ; however, impaction of the first and second molars is rare. In the present case of an impacted second molar, there was probably no relationship to the erupted space. Before the eruption of a tooth, the enamel epithelium is gradually reduced and squamous cell metaplasia begins to appear near the top of the cusp. Vertical movement of the tooth toward the oral epithelium is possible, because the connec- tive tissue between the oral epithelium and REE is broken down and digested by the cells of the REE141.One of the causes of in the present case may have been lack of digestion of the connective tissue due to fibrous hyperplasia of the dental follicle. It is not unusual for nests of the odontogenic epithelium and calcification to be present in the pericoronal tissue of impacted teeth[5-71. The epithelial compo- nents of the hyperplastic dental follicle in the present case are thought to have been inactive and reduced. Most of the scattered OER was probably part of the RDL. Calcification was often found adhering to the REE and OER, or scattered in the fibrous connective tissue. Bud-like proliferations and associations of calcified granules at the REE are sometimes seen in impacted teethm. These calcifications are often similar to cementicles. The cells of the dental follicle are important for the formation of , alveolar bone, and the periodontal ligament during tooth developmentm. The presence of calcification in and around the odontogenic epithelium suggests that the epithelium induces the formation of cementum-like hard tissue, in addition to dystrophic calcification. When well circumscribed radiolucent lesions surrounding the crown of an impacted tooth are found by radiographic examination, a clinical diagnosis of dentigerous cyst is often made. Microscopically, hyperplastic dental follicles are well demarcated and have few to numerous odontogenic epithelia in the delicate fibrous connective tissue. They have been occasionally misdiagnosed as odontogenic fibroma, odontogenic myxoma or myxofibroma. BHASKAR[21reported that distinction between odontogenic fibroma and hyperplastic dental follicle was often difficult. Generally, central odontogenic fibromas cause expansion of the jaws and are seen as unilocular or multilocular radiolucencies involving several roots. These radiographic features are similar to those of ameloblastoma[10,11].It is thought that the histopathological features of hyperplastic dental follicle are similar to those of simple central odontogenic fibromam, although the latter is characterized by a 173 tumor mass made up of mature collagen fibers which are usually interspersed with many plump fibroblasts. They are very uniform in their placement and tend to be equidistant from each other[10,11]On the other hand, hyperplastic dental follicle appears as a small cyst by radiography, and histologically the distribution of collagen fibers and fibroblasts is not uniform. Epithelial components of REE and a ribbon-like arrangement of RDL are often seen in addition to scattered epithelial nests in the fibrous connective tissue. Therefore the major factor in differentiating between normal and hyperplastic dental follicles is whether or not the fibrous tissue is hyperplastic in nature. Hyperplastic dental follicle is not a subtype of odontogenic fibroma, in view of the former's sometimes symmetrical or multiple occurrence[12,13],whereas multiple occurrence of odontogenic fibroma is exceeding- ly rare. The cause of hyperplasia of a dental follicle is obscure, although there are several hypotheses regarding its histogenesis, i.e., tooth impaction, formation of supernumerary teeth, chronic inflammation, and general factors in cases of multiple lesions. The results of the present study suggest that an interrelationship exists between impaction of a tooth for a long period and hyperplasia of the dental follicle. References [1] GARDNER,D. G.: The centralodontogenic fibroma: An attempt at clarification,Oral Surg., 50, 425-432,1980 [2] BHASKAR,S. N.: Synopsisof Oral Pathology,6th ed., 128-129,269-273, Mosby Co., St. Louis, 1981 [3] SCHULZE,C.: Developmentalabnormalities of the teeth and jaws. In Thoma's Oral Pathology,Vol. I, 6th ed., 148-154,Mosby Co., St. Louis, 1970 [4] MOSS-SALENTLIN,L. and HENDRICKS-KLYVERT,M.: Dental and Oral Tissues.An Introduc- tion, 3rd ed., 192-195,Lea & Febiger, Philadelphia, 1990 [5] GETTINGER,R: Relationship of odontogenicepithelium to cysticand other diseasesof mouth and jaw, Arch. Clin. Oral Pathol., 4, 198-239,1940 [6] STANLEY,H. R., HAROLD,K. and PANNKUK,E.: Age changesin the epithelialcomponents of follicles(dental sacs) associatedwith impactedthird molars, Oral Surg., 19, 128-139,1965 [7] CUTRIGHT,D. E.: Histopathologicfindings in the third molar opercula, Oral Surg., 41, 215-224,1976 [8] PINDBORG,J. J. and MAGNUSSON,B.: Chapter 8. Eruption of teeth. In Histologyof the , 161-176,Munksgaard, Copenhagen, 1973 [9] MELCHER,A. H.: Periodontal ligament.In Orban's Oral Histologyand Embryology,10th ed., 198-231,S. N. BHASKAREd., Mosby Co., St. Louis, 1986 [10] WESLEY,R. K., WYSOCKI,G. and MINTZ,S. M.: The central odontogenicfibroma. Clinical and morphologicstudies, Oral Surg., 40, 235-245,1975 [11] SHAFER,W. G., HINE,M. K. and LEVY,B. M.: A Textbook of Oral Pathology,4th ed., 294-295,W. B. SaundersCo., Philadelphia, 1983 [12] SANDLER,H. J., NERSASIAN,R. R., CATALDO,E., POCHEBIT, S. and DAYAL,Y.: Multiple dental follicle with odontogenicfibroma-like changes (WHO type), Oral Surg., 66, 78-84,1988 [13] LUKINMAA,P., HIETANEN, J. and AHONEN,P.: Contiguous enlarged dental follicles with histologic features resemblingthe WHO types of odontogenicfibroma, Oral Surg., 70, 313-317,1990