(Radiology. 1999;210:393-397.)
© RSNA, 1999
Prediction of Benign and Malignant Endometrial Disease: Hysterosonographic-Pathologic Correlation
Theodore J. Dubinsky, MD1,
Kristine Stroehlein, MD2,
Yaser Abu-Ghazzeh, MD4,
H. Richard Parvey, MD5 and
Nabil Maklad, MD, PhD3
1 Department of Radiology, University of Washington, Harborview Medical Center, Box 728359, 325 Ninth Ave, Seattle, WA 98104 (T.J.D.)
2 Departments of Pathology (K.S.)
3 Radiology, Obstetrics, Gynecology, and Reproductive Health Sciences (N.M.), University of Texas, Houston
4 Department of Radiology, Amman Hospital, Jordan (Y.A.G.)
5 Department of Radiology, Veterans Affairs Medical Center, St Louis, Mo (H.R.P.).
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Abstract
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PURPOSE: To determine the transvaginal hysterosonographic appearances of benign and malignant endometrial disease.
MATERIALS AND METHODS: From April 11, 1994, through August 1, 1996, a total of 88 women (age range, 25–81 years) underwent transvaginal hysterosonography and histopathologic evaluation of the endometrium after dilation and curettage or after hysterectomy. A benign appearance at transvaginal hysterosonography was defined as a thin endometrium, diffuse smooth endometrial thickening, or a smoothly marginated, homogeneously echogenic, pedunculated endoluminal mass. A suspicious appearance was defined as either irregular thickening of the endometrium or an inhomogeneous endoluminal mass.
RESULTS: Of 88 women, 37 had a benign-appearing endometrium at transvaginal hysterosonography; at histologic examination, 16 had a proliferative endometrium, 12 had a secretory endometrium, six had polyps, two had an inactive endometrium, and one had carcinoma. Of the 51 women with suspicious endometrial appearances, eight had carcinoma, 24 had adenomatous polyps, five had hyperplasia, 11 had fibroids, and three had endometritis. For carcinoma, the sensitivity of transvaginal hysterosonography was 89%, specificity was 46%, positive predictive value was 16%, and negative predictive value was 97%.
CONCLUSION: A thin endometrium or diffuse smooth endometrial thickening is predictive of benign endometrial histologic findings, but all women with endoluminal masses require further histologic evaluation to exclude malignant disease.
Index terms: Genitourinary system, US, 854.12989 • Uterine neoplasms, 854.30 • Uterine neoplasms, US, 854.12989 • Uterus, endometrium, 854.30
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Introduction
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Transvaginal ultrasonography (US) has been shown to be sensitive for detecting endometrial pathologic conditions as diffuse or focal zones of thickening (1–5). Transvaginal hysterosonography is useful when further evaluation of endometrial thickening or displacement by submucosal fibroids is needed or when the endometrium is suboptimally visualized at transvaginal US (6–10). The demonstration or exclusion of an endoluminal mass can affect further diagnostic evaluation or surgery.
To our knowledge, the ability of transvaginal hysterosonography to distinguish between benign and malignant endometrial abnormalities has not been evaluated with histopathologic correlation. For this purpose, we defined criteria for benign and suspicious lesions seen at transvaginal hysterosonography, applied these criteria prospectively to our transvaginal hysterosonographic interpretations, and then correlated all cases with histopathologic findings obtained either at hysterectomy or at dilation and curettage (D&C). From these data, we calculated the predictive values of our criteria for diagnosing malignant endometrial disease.
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MATERIALS AND METHODS
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All women included in this study had vaginal bleeding that was marked enough to warrant further diagnostic evaluation. Pre-, peri-, and postmenopausal women ranging in age from 25 to 81 years underwent aspiration biopsy of the endometrium in the gynecology clinic of our institution (Lyndon Baines Johnson Hospital). Those women with negative findings at aspiration biopsy of the endometrium were referred to the department of radiology for transvaginal US. Women with positive results at aspiration biopsy were not referred for transvaginal US.
After obtaining informed consent, we prospectively interpreted the results from a total of 189 transvaginal hysterosonographic examinations performed at Lyndon Baines Johnson Hospital, Houston, Tex, from April 11, 1994, through August 1, 1996, according to the criteria outlined in the following paragraphs. Institutional review board approval was not obtained because by this time, articles concerning transvaginal hysterosonography had been published, and transvaginal hysterosonography was considered a routine part of the evaluation of our patients. Most US examinations ordered in these women included transvaginal hysterosonography if necessary.
We then retrospectively reviewed the computer-generated pathology reports of all cases and included only those 88 women who had undergone either a D&C or a hysterectomy within 1 month of the transvaginal hysterosonographic examination. The remaining 101 women were excluded from this study because they did not undergo a D&C or hysterectomy.
All transvaginal US examinations were performed on an ultrasonic imager (model XP12, Acuson, Mountain View, Calif; or model SSA-270A, Toshiba America Medical Systems, Tustin, Calif) with 5-MHz and multifrequency (3.5-, 5.0-, and 7.5-MHz) transvaginal transducers. For each case, at least three measurements of endometrial thickness were made by two observers according to the method of Fleischer et al (3), and a mean thickness was calculated. Each image was evaluated for endometrial visibility, homogeneity, cysts, and displacement by submucosal fibroids.
Premenopausal women underwent imaging at least twice, and persistence of an early–proliferative-phase endometrium thicker than 12 mm was an indication for transvaginal hysterosonography. Seven millimeters was considered the upper limit of normal endometrial thickness in peri- and postmenopausal women receiving hormone replacement therapy, and a 5-mm endometrial thickness was used as the upper limit of normal for women not receiving hormone replacement therapy. The technique of transvaginal hysterosonography has been reported previously (6-10).
All transvaginal hysterosonographic images were interpreted by one of the authors (T.J.D. or H.R.P.) according to the following criteria. A benign endometrial appearance at transvaginal hysterosonography was defined as one of the following: (a) a thin endometrium (thickness at transvaginal hysterosonography, <4 mm), (b) diffuse smooth endometrial thickening (thickness, >4 mm), or (c) a smoothly marginated, pedunculated homogeneously echogenic mass projecting into the endometrial canal. A suspicious endometrial appearance was defined as follows: (a) a focal inhomogeneous mass projecting into the endometrial canal or (b) focal endometrial thickening (thickness, >4 mm).
Sensitivity, specificity, and positive and negative predictive values for predicting malignant disease were then calculated.
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RESULTS
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Eighty-eight women underwent transvaginal hysterosonographic examinations in the department of radiology, followed by D&C (37 patients) or hysterectomy (51 patients). Thirty women with a benign-appearing endometrium underwent D&C. Twenty-eight of the 30 patients had diffuse smooth endometrial thickening, and histologic examination revealed that 16 patients of the 28 patients had a proliferative endometrium and 12 patients had a secretory endometrium (Figs 1, 2). Two of the 30 women had a thin endometrium at transvaginal hysterosonography despite an appearance at transvaginal US that suggested a thickened endometrium; they had an inactive endometrium at D&C (Fig 3). Seven women had pedunculated homogeneously echogenic endoluminal masses demonstrated at transvaginal hysterosonography, and all seven women underwent hysterectomy. Histologic examination yielded six adenomatous polyps (Fig 4) and one adenomatous polyp with a focus of carcinoma in situ.
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Figure 1a. (a) Midsagittal transvaginal hysterosonographic image from a 49-year-old woman shows mild irregularity of the endometrium but no endoluminal masses. The high-amplitude echogenic foci producing posterior acoustic shadowing (arrows) are gas inadvertently introduced during the procedure. (b) Photomicrograph of corresponding histologic section shows normally developing glands (arrows) within proliferative endometrium. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 1b. (a) Midsagittal transvaginal hysterosonographic image from a 49-year-old woman shows mild irregularity of the endometrium but no endoluminal masses. The high-amplitude echogenic foci producing posterior acoustic shadowing (arrows) are gas inadvertently introduced during the procedure. (b) Photomicrograph of corresponding histologic section shows normally developing glands (arrows) within proliferative endometrium. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 2a. (a) Transverse transvaginal hysterosonographic image from a 36-year-old woman shows smooth diffuse endometrial thickening. The endometrium (arrows) is more echogenic than that in the proliferative phase, which is a finding consistently seen in a secretory endometrium because of increasing tortuosity of the glandular structures. (b) Photomicrograph of corresponding histologic section shows mature glandular structures (arrows) within a secretory endometrium. (Hematoxylin-eosin stain; original magnification, x400.)
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Figure 2b. (a) Transverse transvaginal hysterosonographic image from a 36-year-old woman shows smooth diffuse endometrial thickening. The endometrium (arrows) is more echogenic than that in the proliferative phase, which is a finding consistently seen in a secretory endometrium because of increasing tortuosity of the glandular structures. (b) Photomicrograph of corresponding histologic section shows mature glandular structures (arrows) within a secretory endometrium. (Hematoxylin-eosin stain; original magnification, x400.)
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Figure 3a. (a) Midsagittal transvaginal hysterosonographic image from a 64-year-old woman shows no apparent endometrial thickening and no endoluminal masses. The scattered echogenic foci (arrow) moved during fluid instillation and represent small gas bubbles. (b) Photomicrograph of corresponding histologic section shows that the endometrium (arrows) is only one cell layer thick over the underlying stroma, consistent with endometrial atrophy. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 3b. (a) Midsagittal transvaginal hysterosonographic image from a 64-year-old woman shows no apparent endometrial thickening and no endoluminal masses. The scattered echogenic foci (arrow) moved during fluid instillation and represent small gas bubbles. (b) Photomicrograph of corresponding histologic section shows that the endometrium (arrows) is only one cell layer thick over the underlying stroma, consistent with endometrial atrophy. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 4a. (a) Transvaginal hysterosonographic image from a 25-year-old woman shows a pedunculated, homogeneous mass (crosshairs) projecting into the endometrial canal. (b) Photomicrograph of corresponding histologic section shows the presence of blood vessels (arrows) within adenomatous-appearing tissue, consistent with a benign adenomatous polyp. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 4b. (a) Transvaginal hysterosonographic image from a 25-year-old woman shows a pedunculated, homogeneous mass (crosshairs) projecting into the endometrial canal. (b) Photomicrograph of corresponding histologic section shows the presence of blood vessels (arrows) within adenomatous-appearing tissue, consistent with a benign adenomatous polyp. (Hematoxylin-eosin stain; original magnification, x40.)
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The remaining 51 women had a suspicious endometrial appearance according to our criteria. Seven underwent D&C procedures; the remaining 44 underwent hysterectomy. At histologic examination, eight women had endometrial carcinoma (Fig 5), 24 had adenomatous polyps, five had hyperplasia (Fig 6), 11 had endoluminal fibroids, and three had endometritis (Fig 7).
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Figure 5a. (a) Transverse transvaginal hysterosonographic image from a 65-year-old woman shows a broad-based irregular mass (arrows) projecting into the endoluminal canal from the posterior uterine wall. (b) Photomicrograph of corresponding histologic section shows numerous large anaplastic cells that have begun to invade the underlying stroma (straight arrows), consistent with a grade 2 endometrial carcinoma. Normal secretory endometrium (curved arrows) is also present in the image. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 5b. (a) Transverse transvaginal hysterosonographic image from a 65-year-old woman shows a broad-based irregular mass (arrows) projecting into the endoluminal canal from the posterior uterine wall. (b) Photomicrograph of corresponding histologic section shows numerous large anaplastic cells that have begun to invade the underlying stroma (straight arrows), consistent with a grade 2 endometrial carcinoma. Normal secretory endometrium (curved arrows) is also present in the image. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 6a. (a) Transverse transvaginal hysterosonographic image from a 53-year-old woman shows multiple inhomogeneous masses (straight arrows) projecting into the endoluminal canal. Synechiae (curved arrow) are also evident. This image initially was interpreted as multiple polyps. (b) Photomicrograph of corresponding histologic section demonstrates enlarged irregular glandular structures (arrows) without cellular atypia, consistent with endometrial hyperplasia without atypia. We subsequently discovered that hyperplasia frequently appears at transvaginal hysterosonography as multiple masses projecting into the endometrial canal. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 6b. (a) Transverse transvaginal hysterosonographic image from a 53-year-old woman shows multiple inhomogeneous masses (straight arrows) projecting into the endoluminal canal. Synechiae (curved arrow) are also evident. This image initially was interpreted as multiple polyps. (b) Photomicrograph of corresponding histologic section demonstrates enlarged irregular glandular structures (arrows) without cellular atypia, consistent with endometrial hyperplasia without atypia. We subsequently discovered that hyperplasia frequently appears at transvaginal hysterosonography as multiple masses projecting into the endometrial canal. (Hematoxylin-eosin stain; original magnification, x40.)
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Figure 7a. (a) Transverse transvaginal US image from a 39-year-old woman shows measurement of the uterine width (crosshairs) and an inhomogeneous thickened endometrium (arrows). (b) Corresponding transverse transvaginal hysterosonographic image shows an irregular inhomogeneous mass (crosshairs) with a sessile attachment to the posterior uterine wall. This image was interpreted as suspicious (suggestive of carcinoma). (c) Photomicrograph of corresponding histologic section shows innumerable polymorphonuclear cells (arrows) evident within all of the glandular structures and within the endometrial stroma, consistent with acute endometritis. No malignant cells were present in any of the specimens. This similarity in appearance of multiple endometrial disease processes causes the positive predictive value of transvaginal hysterosonography to be low. (Hematoxylin-eosin stain; original magnification, x400.)
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Figure 7b. (a) Transverse transvaginal US image from a 39-year-old woman shows measurement of the uterine width (crosshairs) and an inhomogeneous thickened endometrium (arrows). (b) Corresponding transverse transvaginal hysterosonographic image shows an irregular inhomogeneous mass (crosshairs) with a sessile attachment to the posterior uterine wall. This image was interpreted as suspicious (suggestive of carcinoma). (c) Photomicrograph of corresponding histologic section shows innumerable polymorphonuclear cells (arrows) evident within all of the glandular structures and within the endometrial stroma, consistent with acute endometritis. No malignant cells were present in any of the specimens. This similarity in appearance of multiple endometrial disease processes causes the positive predictive value of transvaginal hysterosonography to be low. (Hematoxylin-eosin stain; original magnification, x400.)
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Figure 7c. (a) Transverse transvaginal US image from a 39-year-old woman shows measurement of the uterine width (crosshairs) and an inhomogeneous thickened endometrium (arrows). (b) Corresponding transverse transvaginal hysterosonographic image shows an irregular inhomogeneous mass (crosshairs) with a sessile attachment to the posterior uterine wall. This image was interpreted as suspicious (suggestive of carcinoma). (c) Photomicrograph of corresponding histologic section shows innumerable polymorphonuclear cells (arrows) evident within all of the glandular structures and within the endometrial stroma, consistent with acute endometritis. No malignant cells were present in any of the specimens. This similarity in appearance of multiple endometrial disease processes causes the positive predictive value of transvaginal hysterosonography to be low. (Hematoxylin-eosin stain; original magnification, x400.)
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The three women with endometritis were 35, 37, and 41 years of age. None of these women had a history of fevers or leukocytosis, but all eventually had positive cultures for chlamydia at subsequent clinical examinations. Eight (15%) of 55 suspicious lesions seen at transvaginal hysterosonography were malignant. The youngest patient with a carcinoma was 35 years old, two cases of carcinoma occurred in women aged 45 and 47 years, and the remaining women with carcinoma were all older than 50 years of age.
Our classification system for detecting endometrial carcinoma at transvaginal hysterosonography had a sensitivity of 89% (eight of nine cases), specificity of 46% (36 of 79 cases), positive predictive value of 16% (eight of 51 cases), and negative predictive value of 97% (36 of 37 cases).
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DISCUSSION
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Eight of nine carcinomas (excluding the one carcinoma in situ), 24 of 31 adenomatous polyps, all 11 endoluminal fibroids, and all three cases of endometritis had the appearance of a focal, inhomogeneous endoluminal mass at transvaginal hysterosonography. The five cases of hyperplasia had a multifocal appearance. The demonstration of an inhomogeneous endoluminal mass is not specific for predicting malignant disease, thus the low positive predictive value of our classification system. We have demonstrated that most marked pathologic abnormalities of the endometrium, including carcinoma, appear as a focal mass at transvaginal hysterosonography. These results also suggest that a directed biopsy procedure may be indicated whenever a suspicious lesion is seen at transvaginal hysterosonography.
Many varying pathologic conditions have similar appearances at transvaginal hysterosonography; endometritis and carcinoma were strikingly similar in our series. However, because carcinoma tends to occur in older women and endometritis in younger women, some differentiation may possibly be made between similar-appearing lesions at transvaginal hysterosonography on the basis of the age, menopausal status, and other risk factors specific for each woman.
All 28 women with diffuse endometrial thickening at transvaginal hysterosonography had either a secretory endometrium or a proliferative endometrium at histologic examination. Six of seven benign-appearing masses were benign adenomatous polyps at histologic examination; however, we did have one carcinoma in situ. Had we included all polypoid masses as suspicious lesions, transvaginal hysterosonography would have had a 100% sensitivity (nine of nine cases) for detecting carcinoma. Women undergoing evaluation for dysfunctional bleeding who have an endoluminal mass demonstrated at transvaginal hysterosonography will have the mass removed to stop the bleeding, whether it appears benign or suspicious. Although the negative predictive value of our classification system is fairly high, the prevalence of malignant disease was low (nine of 88 cases [10%]). Consequently, until more patients with carcinoma are evaluated with transvaginal hysterosonography, the low false-negative rate of transvaginal hysterosonography must be considered preliminary data.
On occasion, differentiation of a fibroid from other suspicious lesions can be difficult because fibroids are also inhomogeneous and sometimes irregular, which would classify them as suspicious in our classification system. Rarely, a fibroid will be so heavily calcified that it is very homogeneously echogenic at transvaginal hysterosonography and would be classified as benign with our criteria.
Another limitation of our study is that some of the histopathologic correlations were obtained after surgical D&C procedures (37 of 88 patients). Thirty of 37 women with a benign endometrial appearance at transvaginal hysterosonography underwent D&C, compared with only seven of 51 women with a suspicious endometrial appearance. For years, the results of D&C were considered to be the standard against which endometrial biopsy results were judged, and only recently, particularly with the development of hysteroscopy, have doubts been raised about the efficacy of D&C (11). Most of the limitations of D&C are due to incomplete sampling of the endometrium or due to mobile polyps that are missed with the curet. In our patients, when a focal mass was seen at transvaginal hysterosonography, the D&C always yielded abnormal histologic findings. We believe that these pathologic findings from D&C were probably more accurate than they would have been had the D&C procedures been performed blindly without knowledge of the transvaginal hysterosonographic results.
We have demonstrated that many endometrial pathologic conditions, particularly hyperplasia and carcinoma, are focal in appearance at transvaginal hysterosonography. Our criteria were highly predictive for benign endometrial processes, particularly diffuse endometrial thickening. Many differing pathologic conditions had a suspicious appearance with our criteria; hence, the positive predictive value of transvaginal hysterosonography for carcinoma was low. On the basis of these preliminary data, we suggest that women with multifocal or sessile lesions should undergo a guided biopsy procedure and that benign-appearing polyps should also be removed to control bleeding and to eliminate the risk of a rare carcinoma in situ. Women with benign endometrial disease seen at transvaginal hysterosonography can probably be safely followed up with transvaginal US, and subjecting them to more invasive diagnostic procedures seems unnecessary. Hence, the role of transvaginal hysterosonography should be to designate patients for more invasive therapy if an endometrial lesion is detected or for medical therapy if none is present.
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Footnotes
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Address reprint requests to T.J.D.
From the 1997 RSNA scientific assembly.
Abbreviation: D&C = dilation and curettage
Author contributions: Guarantor of integrity of entire study, T.J.D.; data acquisition, Y.A.G., H.R.P.; manuscript preparation, K.S., Y.A.G., H.R.P., N.M.
Received December 4, 1997;
revision requested March 6, 1998; revision received June 25, 1998;
accepted August 24, 1998.
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TOP
Abstract
Introduction
