Received, June 29, 1904; accepted for publication

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1 THE AMEBICAN JOURNAL OF CLINICAL PATHOLOGY Copyright 1964 by The Williams & Wilkins Co. Vol. 42, No. 0 Printed in U.S.A. CARCINOMA IN SITU OF THE ENDOMETRIUM ISABELLE A. BUEHL, M.D., PRANK VELLIOS, M.D., JAMES E. CARTER, M.D., AND CARL P. HUBER, M.D. Departments of Pathology and Obstetrics and Gynecology, Indiana University School of Medicine, Indianapolis, Indiana The early changes which may precede invasive carcinoma of the endometrium have been variously designated as atypical hyperplasia, marked adenomatous hyperplasia, and carcinoma in situ. The significance of these changes is debatable. In part, the variation in opinions has been associated with differences in criteria for the diagnosis. In some instances, the lesions seen may well be degenerative or hormonally induced. In other instances, the lesions may already be invasive carcinomas. In 1949, Hertig and associates reported 64 cases of earcinomam situ of the endometrium, which they believe is the earliest histologically identifiable stage of endometrial carcinoma. 4 Their criteria for this diagnosis were foci of glands formed of large eosinophilic cells with pale nuclei. These cells had slightly irregular or wrinkled nuclear membranes. There was often cellular disorientation and disparity in the size of cells, as well as duplication of gland lumens within glands. Almost all of these 64 patients had irregular vaginal bleeding. The mean age was 49 years. Six patients developed invasive endometrial carcinoma 1 to 11 years after the diagnosis of carcinoma in situ. Eight patients had coexistent carcinoma in situ and invasive carcinoma. In 14 cases the carcinoma in situ was present in endometrial polyps. Received, June 29, 1904; accepted for publication August 31. Dr. Buehl is Senior Clinical Trainee, Cancer Control Program, United States Public Health Service; Dr. Vellios is Professor of Pathology; Dr. Carter is Assistant Professor of Obstetrics and Gynecology; Dr. Huber is Chairman of the Department and Professor of Obstetrics and Gynecology. This paper was presented at the Annual Meeting of the American Society of Clinical Pathologists, Chicago, Illinois, October 1, This study was supported by a grant from the Grant County Cancer Society 594 In a study of prior biopsies of patients with endometrial carcinoma, by Hertig and Sommers, carcinoma in situ was observed most frequently 3 to 5 years prior to the diagnosis of invasive carcinoma. 3 Endometrial polyps and cystic hyperplasia were present most often 6 to 13 years prior to invasive carcinoma. Novak and Rutledge, in 1948, reported 44 cases of what they termed atypical endometrial hyperplasia simulating adenocarcinoma. 7 The microscopic changes seen in these cases were similar to those that Hertig used for the diagnosis of carcinoma in situ. Eight cases were treated with curettage alone. The follow-up on these 8 ranged from 1 to 21 years. All remained well, with the exception of 1 who developed adenocarcinoma of the endometrium 15 years later. None of the 10 cases receiving radiation therapy alone developed adenocarcinoma. The remaining 26 cases were treated with hysterectomy without radiation. All but 1 manifested extensive microscopic changes of atypical hyperplasia in the hysterectomy specimen. A similar study of prior biopsies of 13 cases of endometrial carcinoma was reported by Speert. 9 Eleven of these biopsy specimens, obtained 1 to 18^-2 years before the recognition of endometrial carcinoma, contained abnormal foci which he termed adenomatous or atypical hyperplasia. These foci were characterized by combinations of the following: epithelial budding, tuft formation within the gland lumens, outpouching of the gland walls, crowding of the glands, stratification of the epithelium, and pallor of the stained cells. He concluded that these changes should be regarded as a precancerous lesion in the postmenopausal uterus. Similarly, TeLinde and co-workers, studying curettage specimens from patients who then had endometrial carcinoma in excised

2 Dec ENDOMETRIAL CARCINOMA IN SITU 595 uterine specimens, concluded that many lesions previously diagnosed as atypical hyperplasia or adenomatous hyperplasia are, in fact, carcinoma. 10 They based their opinion upon the frequent finding of atypical hyperplasia or adenomatous hyperplasia in the same endometrium with advanced carcinoma and the histologic transition of these lesions to the more malignant-appearing ones. Copenhaver reviewed 184 cases diagnosed as atypical endometrial hyperplasia, 23 of whom subsequently had additional anatomic material for examination. 1 Eight developed adenocarcinoma, 14 manifested no further abnormal changes, and in 1 case the atypical endometrial changes persisted. Gusberg and Kaplan recently reported 191 cases of what they termed adenomatous hyperplasia of the endometrium. 2 The changes in the group they regarded as "marked adenomatous hyperplasia" are similar to the changes Hertig and associates regarded as carcinoma in situ. Ninety of their patients had hysterectomies, and 18 of these had coexistent carcinoma; 12 contained equivocal lesions. These reports indicate that endometrial changes preceding invasive carcinoma can be detected histologically. A more precise classification of endometrial lesions seems practical, and similar histologic lesions that are not precursors of malignancy, as well as already invasive adenocarcinomas, can be separated from carcinoma in situ of the endometrium. MATERIAL AND FINDINGS Iii this laboratory, 87 cases were classified as either atypical hyperplasia or carcinoma in situ of the endometrium during an 11-year period from 1952 to With certain specific criteria for the diagnosis of carcinoma in situ, the cases were reclassified (Table 1). Not all of the changes were necessarily present. The criteria included cellular as well as histologic abnormalities. The cellular changes were nuclear hyperchromatism and irregularity, clumping of nuclear chromatin, enlarged nucleoli, and cytoplasmic eosinophilia. Cytoplasmic eosinophilia was not always present. When it was present, TABLE l CRITERIA FOR DIAGNOSIS OF CARCINOMA IN SITU OF ENDOMETRIUM Nuclear hyperchromatism Nuclear irregularity in size and shape Clumping of nuclear chromatin Enlarged nucleoli Eosinophilia of the cytoplasm Loss of nuclear polarity Piling up of epithelial cells Intraglandular epithelial bridges but nuclear changes were not noted, the lesion was regarded as benign. Histologic changes included loss of polarity of nuclei, piling up of epithelial cells, and intraglandular epithelial bridges (Figs. 1 and 2). When these changes were found, and the lesion was confined within gland lumens in the usual endometrial architecture, the lesion was designated as carcinoma in situ. When the glands were crowded together with little intervening stroma, the likelihood of stromal invasion was regarded as high, and such lesions were diagnosed as invasive adenocarcinomas. The use of periodic acid-schilt stain and reticulum preparations was not helpful in identifying invasion in our material. Even in frankly invasive carcinomas, such "basement membranes" may be noted. Features encountered which are not necessarily precursors of invasive endometrial carcinoma (Table 2) included tubal metaplasia (.Fig. 3), squamous metaplasia (Figs. 4 and 5), degenerative changes in epithelium in postmenopausal women, regeneration of epithelium after curettage, and adenomatous hyperplasia (Fig. 6). The last term is one we have used to designate an increase in the number of glands in an area of endometrium, sometimes with budding, but without the cellular or histologic criteria of malignancy listed above for carcinoma in situ. Reclassification of the 87 cases resulted in 31 being regarded as carcinoma in situ, 9 as doubtful, and 47 as one of the other lesions listed in the morphologic differential diagnosis. In addition, review of cases previously diagnosed as invasive adenocarcinoma resulted in 3 being reclassified as carcinoma in

3 F I G. 1 (upper left). A gland manifesting t h e changes of endometrial carcinoma in silu. Note especially nuclear changes and piling up of cells. Cytoplasmic eosinophilia was also present. Hematoxylin and eosin. X 340. F I G. 2 (upper right). Two glands manifesting the changes of endometrial carcinoma in situ. Note the nuclear changes and t h e epithelial bridges in the elongated gland. Hematoxylin and eosin. X 275. F I G. 3 (lower left). Tubal metaplasia. N o t e t h e ciliated border of these columnar cells. Cytoplasmic eosinophilia was also present. Hematoxylin and eosin. X 425. F I G. 4 (lower r i g h t ). Intraglandular morales (squamous metaplasia) in benign endometrium. Hematoxylin and eosin. X

4 Dec ENDOMETRIAL CARCINOMA IN SITU 597 TABLE 2 DIFFERENTIAii DIAGNOSIS OF CARCINOMA IN Siru OF ENDOMETRIUM Tubal mataplasia Squamous metaplasia Degenerated epithelium Regenerated epithelium following curettage Adenomatous hyperplasia Early invasive carcinoma situ. These 34 cases form the basis of this study (Table 3). If the uterus was removed, serial blocks of the endometrium were taken, and several sections of each block were examined. Usually, individual endometrial glands were involved, and often in the same uterus several such glands were found widely separated by normal endometrium, suggesting that the change is multicentric. Often the portion of the glands so involved was located in the deeper part of the endometrium. In 1 instance the change was present only in a polyp, and the remainder of the endometrium was apparently normal. Six patients had coexisting cystic hyperplasia of the endometrium. In 3 cases the carcinoma in situ of the endometrium was diagnosed in the hysterectomy specimen only. Two of these patients had no curettage prior to hysterectomy. One had a curettage 6 years previously, and that specimen manifested only endometrium in the early secretory phase of the menstrual cycle. In the remaining 31 cases the original diagnosis of carcinoma in situ was made from the curettage specimen. Twenty-three of the patients of this group had hysterectomies shortly after the diagnosis of carcinoma in situ. Seven of these 23 patients were treated with intracavitary radium prior to the hysterectomy, and none of these 7 hysterectomy specimens had demonstrable residual carcinoma in situ. The remaining 16 hysterectomy specimens, removed without prior irradiation, were studied by means of serial blocks of the endometrium. In 8 of these uteri, there were residual foci of carcinoma in situ (Figs. 7 and 8). Invasive carcinoma was not found in any of the hysterectomy specimens when the hysterectomy was performed shortly after the curettage. In 2 instances, the hysterectomy was delayed, for 1 year and for 3 years, respectively, and invasive adenocarcinoma was present in both of the hysterectomy specimens (Figs. 9 and 10). One patient was treated with intracavitary radium alone, owing to extreme obesity, and 4 patients received no further treatment after the curettage. Three of the latter 4 patients are asymptomatic to date (2-, 4-, and 5-year follow-up, Table 4). The fourth patient was lost to follow-up. The patient treated with radium is asymptomatic after 8 years. One 33-year-old white woman had an endometrial biopsy for infertility. Endometrial carcinoma in situ was present in the biopsy specimen, as well as in the subsequent curettage specimen (Fig. 11). A hysterectomy was not performed, owing to her desire to have children. She subsequently became pregnant but had a spontaneous abortion after 3 months gestation. Within a few months she became pregnant again and delivered a 6 lb., 4 oz. infant. Another curettage specimen obtained 8 months after the delivery again was interpreted as containing foci of endometrial carcinoma in situ (Fig. 12). Clinical Findings The clinical findings in these patients were not striking (Table 5). The ages of the patients ranged from 33 to 75, with a median of 48. Seventeen were between 41 and 50. Their weights varied widely. Of the 2S recorded, 12 weighed more than 160 lb. Five of 29 patients had blood pressures greater than 140 systolic and 90 diastolic. All of the patients were Caucasians. None was Jewish. Three were nulligravid, but 1 of these was not married. Two of the patients were diabetics. The reason for the diagnostic curettage in 30 of the 32 patients was abnormal bleeding, which we assume was from some cause other than the carcinoma in situ. One patient was amenorrheic, and another had the curettage as part of an infertility study. Eight of the patients had received hormone (estro-

5 F I G. 5 (upper left). Proliferation of surface epithelium (? early squamous metaplasia) following curettage. Hematoxylin and eosin. X 200. F I G. 6 (upper right). Adenomatous (glandular) hyperplasia. Hematoxylin and eosin. X 130 F I G. 7 (lower left). Carcinoma in situ, in an endometrial gland (curettage specimen). Hematoxylin and eosin. X 425. F I G. 8 (lower right). Carcinoma in situ (hysterectomy specimen). Same case as Figure 7. Hematoxylin and eosin. X

6 Dec ENDOMETRIAL CARCINOMA IN SITU 599 TABLE 3 RECLASSIFICATION OF CASES OK ABNORMAL ENDOM BTRIA I, EPITII ELI UM Carcinoma in nitti. Doubtful Other Totnl Adenocarcinoma "downgraded" Total cases, carcinoma in situ gens or progesterone) in the recent past, usually for therapy of the bleeding episode which eventually led to the curettage procedure by means of which the carcinoma in situ was found. One patient had x-ray castration 15 years previously, and 1 had intracavitary radium for bleeding from leiomyomas 16 years earlier. Eighteen of the patients had cervical and vaginal cytologic examinations prior to the curettage. In only 1 were abnormal cells observed, but these cells came from a concomitant intraepithelial carcinoma of the cervix. DISCUSSION If these changes are actually precursors of invasive adenocarcinoma of the endometrium, it would seem from these observations that adenocarcinoma of the endometrium is multicentric in origin. The average age of the patients in this series was approximately 6 years less than that for patients with invasive carcinoma, suggesting that the changes may precede the presence of clinically apparent adenocarcinoma of the endometrium by at least that length of time. The 2 instances in which the presence of these changes in the curettage specimens was later followed by invasive adenocarcinoma suggest that these changes are those of carcinoma in situ, and that they may be followed by invasive carcinoma if left untreated. Progesterone has been advocated as therapy for carcinoma in situ by Kistner. 6 Doubts of this are raised when one considers the case reported here in which there was carcinoma in situ before her pregnancy and the changes persisted after delivery. It would seem that the high levels of progesterone during the pregnancy should have cured this patient. At the present time we suggest that endometrial changes comparable with those of intraepithelial carcinoma of the uterine cervix occur, and they can be identified morphologically. Their detection cytologically will probably remain a difficult task. Our findings and those of others are only suggestive, and additional controlled observations are needed before generalizations may be made. SUMMARY A review was made of 86 cases in which abnormal endometrial epithelium was present. With specific criteria for the diagnosis of endometrial carcinoma in situ, 34 of the cases were so classified. The criteria suggested for the diagnosis of endometrial carcinoma in situ, include nuclear hyperchromatism and irregularity, clumping of chromatin, enlarged nucleoli, cytoplasmic eosinophilia, loss of polarity of nuclei, piling up of epithelial cells, and intraglandular epithelial bridges. Features which offer difficulty in the histologic differential diagnosis include tubal metaplasia, squamous metaplasia, degenerative changes in endometrial epithelium, adenomatous hyperplasia, and regeneration of epithelium, especially after a curettage of the endometrial cavity. Similarly, early invasive carcinomas were difficult to distinguish from carcinoma in situ. It is suggested that the term adenomatous hyperplasia be reserved for the change in which there is an increase in the number of glands in an area of endometrium, sometimes with budding, but without the cellular or histologic criteria of malignancy listed above. The significance of this lesion has not been determined. Endometrial carcinoma in situ is a multicentric lesion which may occur deep within, as well as near the surface of, the endometrium. The changes were still present in the hysterectomy specimen in S of the 23 cases in which curettage was followed by hysterectomy. In 2 instances when hysterectomy was delayed for 1 year and for 3 years, respec- 118

7 F i e. 9 (upper left). Carcinoma in situ (curettage specimen). Hematoxylin and eosin. X 400 F I G. 10 (upper right). Invasive endometrial carcinoma (curettage specimen). Same case as Figure 9, 1 year later. Hematoxylin and eosin. X 400. F I G. 11 (lower left). Carcinoma in situ in a 33-year-old infertility patient. Hematoxylin and eosin. X 425. F I G. 12 (lower right). Carcinoma in situ in same patient as Figure 11, following spontaneous abortion and subsequent delivery at term, 6 months prior t o t h e time this curettage specimen was obtained. Hematoxylin and eosin. X

8 Dec ENDOMETRIAL CARCINOMA IjY SITU 601 TABLE 4 CARCINOMA /A T SITU OF ENDOMETRIUM Curettage specimen only obtained Curettage specimen positive, hysterectomy specimen positive Curettage specimen positive, hysterectomy specimen negative Curettage specimen positive, hysterectomy specimen negative following irradiation Curettage specimen negative, hysterectomy specimen positive Hysterectomy specimen only Curettage specimen positive, hysterectomy specimen obtained 1 and 3 years later invasive adenocarcinoma TABLE 5 SUMMARY OP CLINICAL FINDINGS IN CARCINOMA IN SITU OP ENDOMETRIUM Age range, median 48 years Race, all white Weight greater than 160 lb., 12 of 29 Diabetes, 2 Hypertension (140/90), 5 of 29 Nulligravida, 3 (1 not married) Reason for curettage, 30 abnormal bleeding, 1 infertility, 1 amenorrhea Hysterectomy without curettage, 2 Previous irradiation, 2 Hormone therapy, 8 tively, invasive endometrial carcinoma was present in the hysterectomy specimen. The average age of the patients with carcinoma in situ is approximately 6 years less than that of patients with invasive endometrial carcinoma. The clinical findings are not specific. REFERENCES 1. COPENHAVER, E. H.: Atypical endometrial hyperplasia. Obst. & Gynec., 13: S, GUSBERG, S. B., AND KAPLAN, A. L.: Precursors of corpus cancer. IV. Adenomatous hyperplasia as stage 0 carcinoma of the endometrium. Am. J. Obst. & Gynec, 87: , HERTIG, A. T., AND SOMMERS, S. C: Genesis of endometrial carcinoma. I. Study of prior biopsies. Cancer, 2: , HERTIG, A. T., SOMMERS, S. C, AND BENGLOFF, H.: Genesis of endometrial carcinoma. III. Carcinoma in situ. Cancer, 2: , KISTNER, R. W.: Histological effects of progestins on hyperplasia and carcinoma in situ of the endometrium. Cancer, 12: , NOVAK, E. R.: Relationship of endometrial hyperplasia and adenocarcinoma of the uterine fundus. J. A. M. A., 154: , NOVAK, E., AND RUTLEDGE, F.: Atypical endometrial hyperplasia simulating adenocarcinoma. Am. J. Obst. & Gynec, 65: 46-63, SOMMERS, S. C, HERTIG, A. T., AND BENGLOFF, H.: Genesis of endometrial carcinoma. II. Cases 19 to 35 years old. Cancer, 2: , SPEERT, H.: The premalignant phase of endometrial carcinoma. Cancer, 6: , TELINDE, R. W., JONES, H. W., JR., AND GALVIN, G. A.: What are the earliest endometrial changes to justify a diagnosis of endometrial cancer? Am. J. Obst. & Gynec, 66: , 1953.

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