E Queyrat in 1911 as occurring on the glans
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1 ERYTHROPLAKIA OF THE ORAL CAVITY WILLIAM G. SHAFER, DDS,* AND CHARLES A. WALDRON, DDS+ Erythroplakia of the oral cavity is a specific disease entity which must be differentiated from other specific or nonspecific inflammatory oral lesions, although this can only be done in most cases by biopsy. A series of 58 cases of oral erythroplakia has been retrieved from 65,354 consecutively accessioned biopsy-surgical specimens. The disease was found to have no apparent sex predilection (31 males and 27 females) and was most frequently seen during the 6th and 7th decades. The most common site of occurrence in females was the mandibular alveolar mucosa-mandibular gingiva-mandibular sulcus, whereas this was the least common site in males. The floor of the mouth was the most common site in males, followed by the retromolar area in both males and females. The histologic findings emphasized the serious nature of the disease, since 91% of the specimens were either invasive carcinoma, carcinoma in situ, or severe epithelial dysplasia. COWH 36~ , RYTHROPLASIA IS A LESION DESCRIBED BY E Queyrat in 1911 as occurring on the glans penis and representing a premalignant process, because of its frequent ultimate development of carcinoma. It generally appears as a flat or slightly elevated, red, velvety or slightly granular, often glistening, rather sharply circumscribed, asymptomatic plaque; it has been discussed in detail by many authors. Blau and Hyman have published an excellent review of the disease, while Graham and Helwig have recently given a detailed analysis of 100 cases. Over the years, there has been considerable controversy as to whether erythroplasia of a mucosal surface is the same disease process as Bowen s disease of the skin, because of similarities in the histologic appearance of the two conditions. Graham and Helwig have concluded that the two are different entities, based on an analysis of data of series of patients with From the Departments of Oral Pathology, Indiana University School of Dentistry, Indianapolis, IN, and Emory university School of Dentistry, Atlanta, GA. * Distinguished Professor and Chairman, Department of Oral Pathology, Indiana University School of Dentistry. t Professor and Chairman, Department of Oral Pathology, Emory University School of Dentistry. Supported in part by PHS Training Grants No. 5-Tl2- CA8006 and 5-Tl2-CA8001 from the National Cancer Institute. Address for reprints: William G. Sharer, DDS, Dept. of Oral Pathology, Indiana University School of Dentistry, Indianapolis, IN Received for publication luly 31, erythroplasia and with Bowen s disease. This conclusion was based on differences in race, ethnic origin, sex, age, duration, anatomical site, number of lesions, family history, arsenic content of lesions, and especially associated cancer and cause of death. They concluded that erythroplasia is a distinct clinicopathologic entity. Earlier, Gorlin had reviewed the literature on Bowen s disease of the oral cavity and reported an additional 6 cases. Howarth4 also had reported 3 cases of oral Bowen s disease. The clinical descriptions of the lesions in these 6 cases of Gorlin and the 3 cases of Howarth, however, did not appear to resemble erythroplasia. The occurrence of erythroplasia of the oral cavity, with clinical and microscopic features nearly identical to the penile lesions, has been recognized for a number of years. The lesion here is generally termed erythroplakia rather than erythroplasia so as to be analagous to its white patch counterpart leukoplakia, representing the Anglicized version of the French erythroplasie and leukoplasie, respectively. It has been described in various detail in the oral cavity by Sachs and Sachs, Pindborg and his asso~iated,~ Williamson, l4 van Rensburg and Shear, Mashberg and his coworker~,~ Mehta and his associates, and Kramer. Shear has published an excellent review and discussion of erythroplakia of the mouth describing three clinical variations of the lesion: 1) homogeneous erythroplakia, 2) 1021
2 1022 CANCER September 1975 Vol. 36 ing on buccal mucosa, in a survey of 50, persons in India. Four of these nine cases showed histologic epithelial atypia. The case of erythroplakia of the buccal mucosa reported by Williamson and of the maxillary alveolar ridge by van Kensburg and Shear both appear to represent classical examples. In a related study of 158 cases of oral squamous cell carcinoma, Mashberg and his associate~~ found that 143 (91%) had an erythroplastic component, but that only 98 (62%) had a white component. They concluded 3rd 4lh 5th 6th 7th 8th 9th that an asymptomatic erythroplastic (red DECADE OF LIFE velvety) lesion [appears to be] the earliest visible Fit;. I. Occurrence of oral erythroplakia by decade of sign of oral squamous cell carcinoma-invasive or in situ. age and,ex. erythroplakia interspersed with patches of leukoplakia, and 3) granular or speckled erythroplakia (the lesion described earlier by Pindborg as speckled leukoplakia ). Pindborg and his associates studied 35 cases of speckled leukoplakia, the majority of which occurred at the oral commissures, and reported that 14% of these were carcinoma and 51% showed histologic epithelial atypia. Perhaps significantly, it has been reported by Jepsen and Winther that 21 of 23 cases (91%) of speckled leukoplakia showed the presence of Candida albicans by culture of scrapings from the lesion, as contrasted to only 24 of 64 cases (39%) of conventional leukoplakia. There have been frequent suggestions concerning the possible etiologic role of Candida albicans in the development of both speckled leukoplakia and conventional leukoplakia and particularly of the epithelial atypia occurring in some of these cases. However, at present the data are insufficient for any firm conclusion. Mehta and his co-workers reported nine cases of oral erythroplakia, the majority also be- Despite the general recognition that erythroplakia-of both the penis and-the oral cavity is apparently a premalignant disease, there has been no report of any significant series of cases of oral erythroplakia to substantiate histologically the seriousness of the condition. The purpose of this report is to provide such data. MATERIALS AND METHODS The entire files of the tissue diagnosis services of Indiana University School of Dentistry, Department of Oral Pathology, and Emory University School of Dentistry, Department of Oral Pathology were utilized in this study. It was carried out in conjuction with a joint study on oral leukoplakia to be published separately. The periods covered were October 1, 1950 through June 5, 1974 (Indiana) and December 1, 1959 through April 1, 1974 (Emory). The total numbers of consecutive cases accessioned and reviewed for this study were 45,447 (Indiana) and 18,907 (Emory), a total of 64,354 cases. The case history sheets submitted by the practitioner with each tissue specimen were ex- Maxillary mucosa and sulcus hlandibular mucosa and sulcus Palate Buccal mucosa Tongue Floor of mouth Retromolar TOTAL TABLE 1. Location of Erythroplakia by Site and Sex* (ELI and IU Combined) ~~ Males Females ~~ ~ TOTAI No. 90 of males No. % offemales No Yo of TOT:\^ H H 12.5 It3 28. I Total number of sites is greater than total number of cases due to multiple sites of involvement in some instances.
3 No. 3 ORAL ERYTHROPLAKIA Shafer and Waldron 1023 amined individually in order to find all lesions described clinically as such that would fit the category of erythroplakia. This individual reading of every case history in the combined files was necessary, since the data are not cornputerized in either institution. In order that the data from the two institu- tions be comparable, certain ground rules were established. It was decided to include in this study only cases of homogeneous erythroplakia, since so many cases of possible speckled erythroplakia or erythroplakia mixed with leukoplakia had clinical descriptions that precluded the definite establishment of the le- FIG. 2. Oral erythroplakia. Mild epithelial dysplasia. A (top). Low magnification. B (bollom). High magnification.
4 1024 CANCER September 1975 Vol. 36 sion within the category of erythroplakia. These It was also necessary to rule out a large lesions, however, were included in the number of inflammatory lesions which might leukoplakia study. The pure homogeneous also appear as a red patch clinically. Shear has erythroplakias were rather easily identified from discussed the problem of inflammatory lesions the clinical descriptions provided by the prac- clinically resembling erythroplakia; these intitioners. clude Cundidu albicans infection (including den- FIG. 3. Oral erythroplakia. Severe epithelial dysplasia. A (fob). Low rnaenification. B High magnifi-
5 No. 3 ORAL ERYTnROxAKlA Shafer and Waldron 1025 ture stomatitis), tuberculosis, histoplasmosis, RESULTS and other nonspecific miscellaneous lesions. In every accessioned case examined that was There appeared to be no significant described clinically as a red patch, the lesion differences in any of the clinical or microscopic could be placed either in the inflammatory findings between the groups of cases of erythrocategory or in the true erythroplakia category - plakia ~ at. Indiana University or at Emory with- no difficulty. University, except for frequency of occurrence of Fri;. 4. Oral erythroplakia. Carcinoma in riru. A ( up). Low niagniticaiion. B (bollom). 1 liyh magnitication.
6 CANCER September 1975 \'ol. 36 con--dd~ CcNO-OOr? - - In N d c. P- h - h erythroplakia in the total number of cases accessioned. Indiana had a total of 31 cases (18 males and 13 females) of erythroplakia in 45,- 447 accessioned cases (0.068%), while Emory had a total of 27 cases (13 males and 14 females) in 18,907 accessioned cases (0.143%), approximately double the frequency of Indiana. 'I'he combined 58 cases of oral erythroplakia (the largest series yet collected) constituted 0.09% of the 64,354 cases accessioned at the two universities during the time intervals previously described. Thus, erythroplakia of oral mucous membranes is a far less common disease than leukoplakia, its white premalignant counterpart. Oral erythroplakia has no apparent sex predilection (31 males and 27 females) and is most common in the 6th and 7th decades of life (Fig. I). This is in contrast to leukoplakia, where there is commonly a predilection for occurrence in males and where occurrence in the 4th and 5th decades is also very common. The most common site of occurrence of the lesion in males in this study was the floor of mouth, but in females the combined mandibular alveolar mucosa-mandibular gingiva-mandibular sulcus was most common (Table 1). Surprisingly, this latter combined site was the least common site of occurrence in males. The retromolar area in both males and females and the floor of the mouth in females was the next most common site of occurrence. The histologic findings of the 65 biopsies in these 58 cases of erythroplakia documented the seriousness of this disease. For purposes of this study, the categories of severe epithelial dysplasia and carcinoma in situ were combined, since they seem to carry the same prognostic significance and since their separation is difficult if not impossible to achieve consistently. Similarly, the categories of mild and moderate epithelial dysplasia were combined, since we feel that they probably carry the same prognostic significance, although supportive data are not available. Of the 65 biopsy specimens, 33 (51%) were invasive carcinoma, 26 (40%) were carcinoma in situ or severe epithelial dysplasia, and 6 (9%) were mild or moderate epithelial dysplasia (Figs. 2-4). There were no significant differences between males and females in the distribution of these various epithelial alterations (Table 2). DISCUSSION 'l'he term "erythroplakia" of the oral cavity as used in this report and as accepted by most oral
7 No. 3 patholoyists describes the clinical appearance of a red patch of the mucous membrane which does not represent some specific or nonspecific inflammatory lesion. Thus, this term carries no histopathologic connotation. However, in most cases the clinician cannot distinguish with certainty the true erythroplakia as discussed here and the more innocuous inflammatory lesions, thus mandating biopsy. Most, and probably all, cases of true clinical erythroplakia represent some epithelial atypia, ranging from mild epithelial dysplasia to invasive carcinoma. Furthermore, there is no correlation between the clinical appearance of erythroplakia and the histologic findings. Some cases of erythroplakia may be so small and innocuous appearing as to nearly escape detection at the time of the oral examination, and yet histologically represent in- ORAL ERYTHROPLAKIA shafer and Waldron 1027 vasive carcinoma (Fig. 5A-D). The explanation for the red appearance of these lesions clinically is evident microscopically, where one finds the normal surface covering of orthokeratin or parakeratin to be absent, and the connective tissue papillae containing engorged capillaries rising between rete ridges very close to the surface. The dysplastic epithelial changes are similar to those occurring in other dysplastic oral lesions, except that there is generally a failure of the cells to show any significant maturation. Thus, individual cell keratinization, keratin pearl formation, and surface keratinization are almost invariably absent until actual invasion begins, at which time cellular maturation may commence. The clinical appearance of the oral lesions may range from very small ones to very large ones covering considerable surface area, from Flc;. 5. Oral erythroplakia. The lesions are frequently so innocuous and innocent-appearing that they ;ire overlooked. A (top lejt). Lesion of lateral tongue: invasive carcinoma. B (top rtght). Lesion at junction of floor 01 mouth and lingual alveolar mucosa: invasive carcinoma. C (boltom Id!). Lesion in anterior floor of mouth: carcinoma in situ. U (bottom right). Lesion at junction of floor of mouth and ventral tongue: invasivc carcinoma.
8 1028 CANCER September 1975 Vol. 36 very mild reddening of the mucosa to almost a blood-red hue, and from a pure homogeneous erythroplakia to one sprinkled with foci of white ( speckled leukoplakia of Pindborg or speckled erythroplakia of Shear) or intermingled with patches of leukoplakia. Many times the border of the lesion clinically is very sharply circumscribed and delineated from adjacent normal mucosa. Only the pure homogeneous variety has been considered in the report. I he speckled and mixed erythroplakias (leukoplakias) were eliminated from the present study and will be included in a report on leukoplakia to be published separately. We have no explanation for the apparent diflerence in frequency of occurrence of the disease between 1 ndiana University (serving chiefly dental practitioners in the Northcentral United States) and Emory University (serving chiefly dental practitioners in the Southeastern United States). No significant factors were described in the histories accompanying the tissue specimens to give any insight into the etiology of the disease. It is of interest that it occurs somewhat later in life than does leukoplakia, thus sug- gesting that either the etiologic agents in erythroplakia must be operative over a longer period of time than in leukoplakia, or that erythroplakia may be more intimately connected with tissue changes associated with the aging process than in leukoplakia. Neither do we have an explanation for the fact that the combined mandibular alveolar ridgemandibular gingiva-mandibular sulcus location is the most common site of occurrence of erythroplakia in women but the least common site in men. This may very possibly relate to etiologic factors important in this disease process but of which we are totally ignorant. Probably the most important fact arising from this study is the seriousness of these frequently overlooked and many times harmless-appearing lesions. The fact that 91% of the tissue specimens studied represented invasive carcinoma, carcinoma in situ, or severe epithelial dysplasia, the vast majority of which were totally unsuspected by the dentist as being at all serious, should be of grave concern to the clinician and pathologist alike. REFERENCES 1. Blau, S., and Hyman, A. B.: Erythroplasia of Queyrat--/\n evaluation of the nature of the condition based on a critical review of the world literature and an analysis and tabulation of all the published American cases and the material collected from 1933 to 1954 at the Skin and Cancer L nit 01 the New York University Hospital. Acta Dcm. C mereol. 35: , Gorlin, K.,J.: Bowen s disease of.the mucous membrane of the mouth. Oral Surg. 3:35-51, Graham, J. H., and Helwig, E. B.: Erythroplasia of Queyrat-A clinicopathologic and histochemical study. Cunrrr 32: Howarth, M.: Precancerous epitheliomatosis (Bowen s disease) of the palate and fauces. J. Laryngol. 50:28-32, Jepsen, A,, and Winther, J. E.: hlycotic infection in oral leukoplakia. Acta Odontol. Scand. 23: , Kramer, I. K. H.: Carcinoma-in-situ of the oral mucosa. Int. Dent. J. 23:94-99, hlashberg, A., hlorrissey, J. B., and Garfinkel, L.: A study of the appearance of early asymptomatic oral squarnous cell carcinoma. Cancer 32: , Mehta, F. S., Pindborg, J. J., and Hamner, J. E.: Oral Cancer and Precancerous Conditions in India. Copenhagen, Munksgaard, Pindborg, J. J., Kenstrup, G., Poulsen, H. E., and Silverman, Jr., S.: Studies in oral leukoplakias-v. Clinical and histologic signs of malignancy. Acta Odonlol. Scand. 21: , Queyrat, L.: Erythroplasie de gland. Bull. Soc. Fr. Dermatol. Syphiligr. 22: , Sachs, W., and Sachs, P. hi.: Erythroplasia of Queyrat. Arch. Dcrmafol. Syphtlol. 58: , Shear, hl.: Erythroplakia of the mouth. Inl. Dent. J. 22: , van Kensburg, B. C;. J., and Shear, M.: Cranulomatous and granulomatoid lesions of the oral mucosa. J. Dent. Assoc. S. A/r. 21: , Williamson, J. J.: Erythroplasia of Queyrat of the buccal mucous membrane. Oral Surg. 17: , 1964.
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