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Adenomyosis: US Features with Histologic Correlation in an in Vitro Study¹

¹ From the Departments of Radiology (M.A., C.R., P.M.B.) and Pathology (A.R.M.), McGill University, Montreal General Hospital, Quebec, Canada; and the Departments of Pathology (W.B.C.) and Medical Imaging (M.A., P.M.B.), University of Toronto, University Health Network and Mount Sinai Hospital, 610 University Ave, Toronto, Ontario, Canada M5G 2M9. From the 1997 RSNA scientific assembly. Received July 16, 1999; revision requested August 25; revision received October 19; accepted October 26. Address correspondence to M.A. (e-mail: mostafa_atri@pmh.toronto.on.ca).

	Abstract

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
PURPOSE: To evaluate the accuracy of ultrasonographic (US) features of adenomyosis by correlating them with histologic findings and to assess inter- and intraobserver agreement.

MATERIALS AND METHODS: US was performed and videotaped in 102 consecutive hysterectomy specimens in a water bath. Videotapes were reviewed initially by two independent radiologists blinded to the clinical and histologic findings and after 1 month by one of the two; US and histologic findings were correlated. Features evaluated included diffuse abnormal echotexture of myometrium, subendometrial myometrial cysts, subendometrial echogenic nodules, subendometrial echogenic linear striations, nodular endometrial-myometrial junction, poor definition of the endometrial-myometrial junction, asymmetric thickness of the anteroposterior wall of the myometrium, and globular configuration.

RESULTS: The prevalence of adenomyosis in this cohort was 29.4% (30 of 102 specimens). The mean sensitivity, specificity, negative predictive value, positive predictive value (PPV), and accuracy for the diagnosis of adenomyosis for the three reviews were 81%, 71%, 90%, 54%, and 74%, respectively. All findings evaluated, except for nodular endometrial-myometrial junction, were significantly more common in uteri with adenomyosis (P < .05). Heterogeneous myometrium reached borderline significance (P = .05). The specificities and PPVs of subendometrial striations, subendometrial echogenic nodules, and asymmetric myometrial thickness were significantly higher than those of other features (P < .05). The interobserver agreement was moderate ( = 0.48), and the intraobserver agreement was good ( = 0.67) for the three reviews.

CONCLUSION: The presence of subendometrial linear striations, subendometrial echogenic nodules, or asymmetric myometrial thickness improves the specificity and PPV of US in diagnosing adenomyosis.

Index terms: Endometriosis, 854,3192 • Ultrasound (US), tissue characterization, 854.317, 854.3192 • Uterine neoplasms, diagnosis, 854.12981, 854.317, 854.3192 • Uterine neoplasms, US, 854.12981, 854.317, 854.3192 • Uterus, endometrium, 854.317, 854.3192 • Uterus, myometrium, 854.317, 854.3192 • Uterus, US, 854.12981, 854.317, 854.3192

	Introduction

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Adenomyosis is a disease entity diagnosed when endometrial glands and stroma deep in the myometrium are associated with surrounding myometrial hypertrophy (1). The finding classically associated with adenomyosis is excessive uterine bleeding accompanied by worsening dysmenorrhea. However, these findings are often seen in other conditions such as leiomyoma, endometriosis, or endometrial polyps that commonly accompany adenomyosis (2,3). Approximately 650,000 hysterectomies are performed in the United States annually; excessive menstrual blood loss is the single most common indication, accounting for 20% of hysterectomies (4).

The prevalence of adenomyosis, according to published articles on surgical series, varies from 5% to 70% (3). The rate of preoperative diagnosis of adenomyosis on the basis of clinical findings is poor, ranging from 2.6% to 26% (5–8). Endometrial resection or ablation is considered an alternative to hysterectomy for patients with abnormal uterine bleeding. However, the success rate of this procedure is lower when there is deep adenomyosis (9). Reliable diagnosis of adenomyosis is not possible, and adenomyosis cannot be consistently differentiated from leiomyomas with transabdominal ultrasonography (US) (10,11).

The advent of endovaginal US has substantially improved the ability to diagnose adenomyosis. Different US features of adenomyosis have been reported in the literature, including uterine enlargement not explainable by the presence of leiomyomas (12), asymmetric thickening of the anterior or posterior myometrial wall (12–14), lack of contour abnormality or mass effect (12), heterogeneous poorly circumscribed areas within the myometrium (12–16), anechoic lacunae or cysts of varying sizes (13,15–17), and increased echotexture of the myometrium (13,14). Although it has been shown that US diagnosis of adenomyosis is accurate (15) and comparable to MR imaging diagnosis (18), the features are subjective, and to our knowledge inter- and intraobserver agreements have not been evaluated.

We hypothesized that adenomyosis can be accurately diagnosed with a high-frequency transducer by using some previously described features and some additional findings we have observed. The objective of our study was (a) to evaluate the accuracies of using previously described US findings and some additional US features to diagnose adenomyosis in an in vitro setting by correlating these features with the histologic findings and (b) to assess the inter- and the intraobserver agreements for the US diagnosis of adenomyosis.

	MATERIALS AND METHODS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Study Design
We prospectively examined consecutive intact hysterectomy specimens in vitro with high-frequency US. We chose an in vitro setting to allow us better correlation of US features and histologic findings. In addition, the in vitro setting allows less biased evaluation of intra- or interobserver agreement for the findings because the operator-dependent scanning bias of in vivo US is absent.

Study Population
Specimens with substantial distortion because of the presence of leiomyomas at gross inspection and those requiring frozen section were excluded. One hundred six consecutive specimens were scanned between May 1994 and July 1996. Four were eliminated because of substantial distortion of the myometrium by deep leiomyomas identified at US examination. Therefore, the study population consisted of 102 hysterectomy specimens. Sixty-two uteri were postmenopausal, and 40 were premenopausal.

The demographics and clinical data were collected by means of retrospective chart review. The patient age ranged from 22 to 85 years (mean age, 51 years). The dominant features at presentation were uterine prolapse (n = 14), urinary incontinence (n = 7), premenopausal abnormal uterine bleeding (n = 11), premenopausal abnormal uterine bleeding and dysmenorrhea (n = 20), dysmenorrhea (n = 1), pelvic pain (n = 5), postmenopausal bleeding (n = 3), suspicious endometrial biopsy findings (n = 11), abnormal Papanicolaou test results (n = 6), adnexal mass (n = 15), dysmenorrhea and adnexal mass (n = 2), premenopausal abnormal uterine bleeding and adnexal mass (n = 2), transsexuality (n = 2), and familial ovarian cancer (n = 3). The final histologic diagnoses are listed in Table 1.

All US examinations were videotaped for future review. Two experienced radiologists (M.A., C.R.) reviewed the videotaped US examinations independently at the termination of the study while blinded to the histologic results and clinical history.

One of the reviewers (M.A.) reviewed the videotapes for a second time with a 1-month interval between the two reviews. The following US criteria were evaluated: diffuse abnormal echotexture of myometrium (predominantly hypoechoic or heterogeneous), subendometrial myometrial cysts, subendometrial echogenic nodules, subendometrial echogenic linear striations, nodular endometrial-myometrial junction, poor definition of the endometrial-myometrial junction, asymmetry of the anteroposterior wall of the myometrium, and globular rounded configuration of the uterus. Each reviewer was asked to determine the presence of each criterion and use a three-point scoring system for the final diagnosis (score of 1 = negative, 2 = indeterminate, 3 = positive). The extent of disease was categorized as less than one-third, less than two-thirds, or more than two-thirds of the myometrial thickness. In addition, the site of involvement was recorded as anterior, posterior, or both. The thickness of the subendometrial halo was measured in all uteri at real-time examination.

Histologic Examination
Hysterectomy specimens were cut in the sagittal plane at 1-cm intervals. The same pathologist (A.R.M.) initially reviewed all pathologic specimens while blinded to the US and clinical findings. She obtained further thinner cuts to look at the histologic correlation with the US features. For the second histologic review, the information provided included the site (anterior, posterior, both) and the extent of involvement. The pathologist determined the presence of adenomyosis and the site and extent of involvement by following the same format as the US reviewers.

At histologic examination, the presence of multiple patches of or diffuse areas of endometrial glands and/or stroma associated with surrounding muscle hypertrophy located more than halfway from the endometrial-myometrial junction when looking at the specimen with a low-power lens on the microscope was considered diagnostic of adenomyosis.

Statistical Analysis
Descriptive analysis was performed by using proportions, means, SDs, and ranges. Sensitivity, specificity, negative predictive value (NPV), positive predictive value (PPV), and accuracy were determined for the individual finding and the final diagnosis for each reviewer. To investigate differences in the thickness of the subendometrial halo between the group with and the group without histologically proved adenomyosis, Student t tests were employed. The Fisher exact test was used for the comparison of the categorical variables; 95% CIs were calculated by using the approximation by Woolf.

The Mann-Whitney test for nonparametric data was used to investigate differences between the sensitivity and specificity of diagnosing adenomyosis by the two reviewers. statistics were used to calculate inter- and intraobserver agreement and to analyze US-histologic correlation. A statistic of less than 0.40 indicated poor agreement; 0.40–0.59, moderate agreement; 0.60–0.74, good agreement; and greater than or equal to 0.75, excellent agreement (19).

	RESULTS

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Adenomyosis was present in 30 (29.4%) of the 102 specimens at the histologic examination. The prevalence was 26% (16 of 62) in the postmenopausal uteri and 35% (14 of 40) in the premenopausal uteri. The difference was not statistically significant (P > .05).

Table 2 lists the sensitivity, specificity, NPV, PPV, and accuracy of the two readings by reviewer 1 and the reading by reviewer 2 for the final diagnosis of adenomyosis. Since there were a few indeterminate readings (score of 2) for each reviewer, sensitivity analysis was performed to determine the best and worst results. The best result was calculated with all indeterminate cases counted as correct US diagnoses, and the worst result was calculated with all indeterminate cases counted as incorrect US diagnoses. There was no significant difference in the values for the best and worst results. These results were not significantly different from the results obtained after eliminating the indeterminate cases. The numbers in Table 2 are the means of the best and worst results.

The statistics showed moderate agreement for the interobserver agreement and good agreement for the intraobserver agreement (Tables 3, 4). There was good agreement between both reviewers' readings and histologic findings of the depth of myometrial involvement (Table 5). The agreement was excellent between the two reviewers for the determination of the depth of involvement (Table 6).

Only subendometrial echogenic nodules, subendometrial linear striations, and asymmetric myometrial thickness resulted in specificities and PPVs equal to or beyond the 95% CI range of the mean of all findings (Table 8). The thickness of the subendometrial halo in the adenomyosis group was 0–8 mm (mean, 2.5 mm) whereas that in the nonadenomyosis group was 0–6 mm (mean, 1.5 mm). The difference in the means of the two groups did not reach statistical significance (P = .06).

There were two false-negative cases by combining the readings of the two reviewers. The first case was patchy involvement of the inner third of an atrophic postmenopausal uterus; the second case was diffuse involvement but no substantial muscle hypertrophy.

There were 19 false-positive cases by combining the readings of the two reviewers. Six cases were muscle hypertrophy without endometrial glands; two were endometrial carcinomas with superficial invasion; four were basal layer cysts that extended into the underlying muscle; one represented multiple small fibroids; and in six, no cause could be determined.

	DISCUSSION

TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 
Islands of adenomyosis may be scattered throughout the uterine musculature, which gives origin to the diffuse form of the disease; less frequently, they occur in a localized form, the so-called adenomyoma (1,20). In our series, the prevalence of adenomyosis was 26% (16 of 62) in the postmenopausal uteri as compared to 35% (14 of 40) in the premenopausal uteri, with no significant difference between the two groups. The wide range of reported prevalences of adenomyosis in surgical specimens is related to the difference in the criteria used to diagnose adenomyosis, in terms of acceptable depth from the endometrial-myometrial junction and the thickness of sectioning of the uterus (3). In one series, the diagnostic rate in the same uteri varied between 31% and 62%, depending on the number of samples obtained (21). Although adenomyosis is seen in both symptomatic patients and asymptomatic patients, it appears to be more common in symptomatic patients (3,22).

The variable appearance of adenomyosis at US relates to the distribution of the heterotopic endometrial tissue, the presence and degree of associated muscle hypertrophy, and the presence and size of the cysts within the heterotopic endometrial tissue. In our prospective in vitro study, we evaluated the accuracies of previously described features of adenomyosis and of some additional findings we had observed in vivo to determine the histologic explanation for these findings and the inter- and intraobserver agreements for the final diagnoses. The additional features included subendometrial echogenic linear striations (Fig 1), subendometrial echogenic nodules (Fig 2), poor definition of the endometrial-myometrial junction (Fig 1), and nodular endometrial-myometrial junction (Fig 3). In addition, we included previously described features of subendometrial cysts (Fig 2), diffuse hypoechoic or heterogeneous architecture of the myometrium (Figs 3–5), asymmetry of the anteroposterior wall (Figs 5, 6), and globular configuration (Fig 2) of the uterus.

View larger version (107K): [in this window] [in a new window] [Download PPT slide]   Figure 1a. True-positive diagnosis of adenomyosis in a specimen from a 68-year-old woman with vaginal bleeding. (a) In vitro US image demonstrates extensive heterogeneous adenomyosis of the inner two-thirds of the myometrium. Note the echogenic linear striations (arrowheads) surrounded by hypoechoic myometrium. The endometrium is poorly defined throughout its outer contour, and there is evidence of a mild mass effect on the endometrium (arrow). (b) Corresponding low-power microscopic section shows multiple small endometrial islands (arrowheads) in the myometrium surrounded by muscle hypertrophy (solid arrow), which corresponds to the small echogenic linear striations. The open arrow indicates the endometrial surface of the uterus. (Hematoxylin-eosin stain; original magnification, x4.8.)

View larger version (99K): [in this window] [in a new window] [Download PPT slide]   Figure 1b. True-positive diagnosis of adenomyosis in a specimen from a 68-year-old woman with vaginal bleeding. (a) In vitro US image demonstrates extensive heterogeneous adenomyosis of the inner two-thirds of the myometrium. Note the echogenic linear striations (arrowheads) surrounded by hypoechoic myometrium. The endometrium is poorly defined throughout its outer contour, and there is evidence of a mild mass effect on the endometrium (arrow). (b) Corresponding low-power microscopic section shows multiple small endometrial islands (arrowheads) in the myometrium surrounded by muscle hypertrophy (solid arrow), which corresponds to the small echogenic linear striations. The open arrow indicates the endometrial surface of the uterus. (Hematoxylin-eosin stain; original magnification, x4.8.)

View larger version (112K): [in this window] [in a new window] [Download PPT slide]   Figure 2. True-positive diagnosis of adenomyosis in a specimen from a 41-year-old woman with a history of menorrhagia. In vitro US image demonstrates extensive heterogeneous adenomyosis of the inner two-thirds of the myometrium. Note the small echogenic nodules (arrowheads) surrounded by hypoechoic myometrium. A subendometrial cyst (arrow) is posteriorly separated from the thin endometrium by myometrial tissue.

View larger version (155K): [in this window] [in a new window] [Download PPT slide]   Figure 3. True-positive diagnosis of adenomyosis in a specimen from a 62-year-old woman with postmenopausal bleeding and findings of atypia at endometrial biopsy. In vitro US image shows irregular hypoechoic areas of the inner myometrium, with an undulating outer contour of the endometrium (arrowheads).

View larger version (154K): [in this window] [in a new window] [Download PPT slide]   Figure 4. True-positive diagnosis of adenomyosis in a specimen from a 59-year-old woman with a history of stress incontinence. In vitro US image shows adenomyosis of the myometrium that manifests as a predominantly hypoechoic inner half of the myometrium. Note the poor definition of the outer contour of the endometrium (arrowheads).

View larger version (106K): [in this window] [in a new window] [Download PPT slide]   Figure 5. True-positive diagnosis of adenomyosis in a specimen from a 54-year-old woman with a previous history of hypermenorrhea who underwent hysterectomy and bilateral salpingo-oophorectomy because of a large ovarian dermoid. In vitro US image shows a large area of heterogeneous architecture (arrowheads) in the anterior part of the myometrium that contains hypo- and hyperechoic zones. Note the mild mass effect disproportionate to the size of the abnormal area on the anterior aspect of the endometrium (arrows).

View larger version (140K): [in this window] [in a new window] [Download PPT slide]   Figure 6a. True-positive diagnosis of adenomyosis in a specimen from a 49-year-old woman with a long history of menometrorrhagia. (a) In vitro US image shows diffuse adenomyosis of one wall (arrowheads) with a diffusely heterogeneous coarse architecture and multiple edge shadows. Notice the poor definition of the abnormal area of the myometrium and the relatively mild mass effect on the endometrium (arrows). (b) Corresponding low-power microscopic section demonstrates replacement of the whole normal myometrium by multiple endometrial islands separated by whorls of muscle hypertrophy (arrowheads), the explanation for the edge shadows. The arrow indicates the endometrial surface of the uterus. (Hematoxylin-eosin stain; original magnification, x5.8.)

View larger version (126K): [in this window] [in a new window] [Download PPT slide]   Figure 6b. True-positive diagnosis of adenomyosis in a specimen from a 49-year-old woman with a long history of menometrorrhagia. (a) In vitro US image shows diffuse adenomyosis of one wall (arrowheads) with a diffusely heterogeneous coarse architecture and multiple edge shadows. Notice the poor definition of the abnormal area of the myometrium and the relatively mild mass effect on the endometrium (arrows). (b) Corresponding low-power microscopic section demonstrates replacement of the whole normal myometrium by multiple endometrial islands separated by whorls of muscle hypertrophy (arrowheads), the explanation for the edge shadows. The arrow indicates the endometrial surface of the uterus. (Hematoxylin-eosin stain; original magnification, x5.8.)

All the findings evaluated, with the exception of a nodular endometrial-myometrial junction, were significantly more common in the adenomyosis group than in the nonadenomyosis group. Among all the findings evaluated, subendometrial linear striations, subendometrial echogenic nodules, and asymmetric myometrial thickness resulted in the best specificity and PPV (Table 8). Therefore, these findings should be sought to increase the specificity of US.

In our series, the interobserver agreement was moderate ( = 0.48) and the intraobserver agreement was good ( = 0.67).

Good agreement was present between the readings of the two reviewers and histologic findings ( = 0.67 and 0.70), and excellent agreement was present between the two reviewers for the prediction of the depth of involvement ( = 0.94). This could be valuable information in predicting the response to endometrial ablation since it appears that patients with abnormal uterine bleeding and deep adenomyosis do not respond as well to endometrial ablation (9).

There appeared to be close correlation between the US features of adenomyosis and the histologic findings. The areas of increased echotexture corresponded to the islands of endometrial glands, and hypoechoic areas corresponded to the associated muscle hypertrophy (Figs 1, 2, 5). In fact, the combination of the echogenic and hypoechoic areas facilitated the US diagnosis of this condition, as was suggested by the absence of substantial muscle hypertrophy in the two false-negative diagnoses in this series. In extreme cases of muscle hypertrophy, edge shadows were seen in specimens with adenomyosis (Fig 6), presumably because of whorls of muscle bundles, as is described in patients with uterine fibroids (24). Lack of a distinct margin and no mass effect or a mild mass effect disproportionate to the size of the abnormal area helped differentiate adenomyosis from uterine fibroids (Fig 6).

False-positive cases were due to hypoechoic myometrium secondary to either muscle hypertrophy without associated endometrial glands or atrophic myometrium (Fig 7), basal layer cysts extending into the underlying muscle (Fig 8), subendometrial echogenic nodules due to endometrial carcinoma with superficial invasion (Fig 9), and multiple small uterine fibroids. Prominent subendometrial spiral arteries may mimic linear striations of adenomyosis and may help explain some false-positive cases without an explanation. Cases of diffuse hypoechoic areas in the myometrium due to muscle hypertrophy with no endometrial glands may represent inactive adenomyosis. In the absence of echogenic nodules, these cases cannot be differentiated from adenomyosis. The thick nature of the hypoechoic zone helps differentiate it from the thin normal subendometrial halo.

View larger version (115K): [in this window] [in a new window] [Download PPT slide]   Figure 7. False-positive diagnosis of adenomyosis in a specimen from a 56-year-old woman with uterine prolapse. In vitro US image shows diffuse hypoechoic areas (arrowheads) in the inner half of the myometrium and a thin endometrium (arrow).

View larger version (159K): [in this window] [in a new window] [Download PPT slide]   Figure 8a. False-positive diagnosis of adenomyosis in a specimen from a 69-year-old woman with uterine prolapse. (a) In vitro US image shows two cysts (arrowheads) in the subendometrial myometrium. However, note that these cysts abut the outer contour of the endometrium. (b) Corresponding low-power microscopic section shows that these cysts (arrowheads) are all in continuity with the endometrium. The arrow indicates the endometrial surface of the uterus. (Hematoxylin-eosin stain; original magnification, x6.4.)

View larger version (122K): [in this window] [in a new window] [Download PPT slide]   Figure 8b. False-positive diagnosis of adenomyosis in a specimen from a 69-year-old woman with uterine prolapse. (a) In vitro US image shows two cysts (arrowheads) in the subendometrial myometrium. However, note that these cysts abut the outer contour of the endometrium. (b) Corresponding low-power microscopic section shows that these cysts (arrowheads) are all in continuity with the endometrium. The arrow indicates the endometrial surface of the uterus. (Hematoxylin-eosin stain; original magnification, x6.4.)

View larger version (126K): [in this window] [in a new window] [Download PPT slide]   Figure 9. False-positive diagnosis of adenomyosis due to superficial invasion by endometrial carcinoma in a specimen from a 55-year-old woman with postmenopausal bleeding. In vitro US image shows a subendometrial echogenic nodule (arrow), which at histologic analysis corresponded to a superficially invasive adenocarcinoma of the endometrium.

View larger version (173K): [in this window] [in a new window] [Download PPT slide]   Figure 10. Adenomyoma of the uterus in a specimen from a 61-year old woman who had undergone hysterectomy and salpingo-oophorectomy for ovarian cancer. In vitro US image shows a well-defined peripheral hypoechoic mass (arrow) that at histologic analysis was confirmed to be adenomyoma.

In conclusion, inter- and intraobserver agreement for US diagnosis of adenomyosis was moderate to good. Among the previously published findings and the findings evaluated in our series, subendometrial linear striations, subendometrial echogenic nodules, and asymmetric myometrial thickness demonstrated the best specificities and PPVs in the diagnosis of adenomyosis.

	Acknowledgments

 
We express our appreciation to Heidi Van Alstyne for her assistance in the preparation of this manuscript.

	Footnotes

 
Abbreviations: NPV = negative predictive value, PPV = positive predictive value

Author contributions: Guarantor of integrity of entire study, M.A.; study concepts and design, M.A.; definition of intellectual content, M.A., P.M.B., C.R.; literature research, M.A.; experimental studies, M.A., C.R., A.R.M.; data acquisition, M.A., C.R.; data analysis, M.A.; statistical analysis, M.A.; manuscript preparation, M.A., A.R.M., W.B.C.; manuscript editing and review, M.A., C.R., P.M.B.

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TOP Abstract Introduction MATERIALS AND METHODS RESULTS DISCUSSION References

 

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