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(Radiology. 1999;210:739-745.)
© RSNA, 1999


Genitourinary Imaging

Endometriomas: Diagnostic Performance of US

Maitray D. Patel, MD1, Vickie A. Feldstein, MD1, Dillon C. Chen, MD1, Scott D. Lipson, MD1 and Roy A. Filly, MD1

1 Department of Radiology, University of California, San Francisco.


    Abstract
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To determine the diagnostic performance of specific ultrasonographic (US) features in discriminating endometriomas from other adnexal masses.

MATERIALS AND METHODS: Two sonologists independently reviewed the sonograms of 252 adnexal masses in 226 women and recorded US features by using a standardized checklist. The diagnostic performance of specific US features and overall reviewer impression in discriminating endometriomas from other adnexal masses were evaluated.

RESULTS: There were 40 endometriomas. Diffuse low-level internal echoes were present in 38 (95%) endometriomas and 40 (19%) nonendometriomas (positive likelihood ratio, 5). The positive likelihood ratio for the diagnosis of endometrioma increased to 8 if masses with neoplastic features at gray-scale US were excluded, allowing identification of 30 endometriomas (75%). The presence of multilocularity or hyperechoic wall foci further increased the positive likelihood ratio to 48, allowing the identification of 18 endometriomas (45%).

CONCLUSION: An adnexal mass with diffuse low-level internal echoes and absence of particular neoplastic features is highly likely to be an endometrioma if multilocularity or hyperechoic wall foci are present. A patient with a mass with diffuse low-level internal echoes and other US features may benefit from additional imaging.

Index terms: Dermoid, 85.313 • Endometriosis, 85.3192 • Ovary, neoplasms, 852.31, 852.319, 852.32 • Pelvic organs, abnormalities, 85.1493 • Pelvic organs, diseases, 85.2172 • Pelvic organs, neoplasms, 85.31, 85.32 • Pelvic organs, US, 85.1298


    Introduction
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Endometriomas manifest diverse ultrasonographic (US) appearances, ranging from anechoic to echogenic cysts to masses containing multiple septations and solid tissue (1,2). At least four groups of investigators have previously explored the diagnostic performance of US in identifying and distinguishing endometriomas from other adnexal masses (38). Unfortunately, each group tested different sets of US criteria. Moreover, none of these studies sought to determine which set of US criteria yielded the highest diagnostic performance in identifying endometriomas.

We designed our study to determine which combination of gray-scale US features has the highest diagnostic value in distinguishing endometriomas from other adnexal masses and to quantify the diagnostic performance of gray-scale US in this regard. This information helps establish the diagnostic power of gray-scale US for making a diagnosis of endometrioma, which would then serve to discriminate which subgroups of patients with endometriomas, if any, would benefit from additional diagnostic testing (46,810).


    MATERIALS AND METHODS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The study consisted of a retrospective review of the sonograms from 226 women with 252 adnexal masses. The patients were selected from two distinct groups. In the first cohort, we conducted a review of 1,170 consecutive patients who underwent pelvic US at one institution (San Francisco General Hospital, Calif) between June 1993 and August 1994. This yielded 233 ultrasonographically identified adnexal masses in women who were not suspected of having an ectopic pregnancy or pelvic inflammatory disease. From these, 103 masses had a diagnosis established by means of histopathologic evaluation (n = 65) or follow-up US that demonstrated resolution of the mass (n = 38). The latter were all considered to represent nonneoplastic cysts, with hemorrhage if echoes were present within the cyst.

The second cohort was selected from a retrospective review of data from nonconsecutive patients who had undergone pelvic US at one of two institutions (San Francisco General Hospital and University of California Hospital, San Francisco) and in whom an ultrasonographically identified adnexal mass had been surgically excised and histopathologically examined (n = 149).

Cohort 1 ensures that US findings related to endometriomas are compared with the entire spectrum of abnormal adnexal processes, including self-limiting abnormalities. Cohort 2 serves to increase the number of cases analyzed to ensure greater variability in the appearance of endometriomas and to promote comparison with other adnexal processes, particularly malignant lesions.

Two sonologists (R.A.F., V.A.F.) blinded to the clinical history of the patient, the information about follow-up examinations, and the final diagnosis independently reviewed each sonogram. For each mass, both sonologists recorded US features by using a standardized checklist that contained the following observations: focal acoustic impedance (Fig 1), regional bright echoes (Fig 1), hyperechoic lines and dots, fluid-fluid level (gravity-dependent linear interface between two materials of differing echogenicity), fibrinous strands (pattern of fine interdigitating lines that yield a fishnet appearance) (Fig 2), retracting clot (marginal clumped echoes with concave margins), diffuse low-level internal echoes (Figs 19), and hyperechoic wall foci (punctate peripheral echogenic foci) (Figs 4, 5). Masses were categorized as cystic on the basis of demonstration of a definable wall and increased acoustic transmission. For those masses that had cystic US features, reviewers were asked to determine whether septations were present (Fig 6), to characterize wall and septation thickness (by using subjective assessment of images, with 3 mm as the distinction between thin and thick), and to characterize wall and septation contour as smooth, irregular, or nodular (Figs 79). For the purposes of data analysis, a mass was considered to exhibit a listed US feature if at least one of the reviewers designated the presence of that feature. For any given mass, when the feature checklist differed between the two reviewers, no attempt was made to reach a consensus opinion with regard to the presence of a feature.



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Figure 1. Cystic teratoma of the right ovary in a 32-year-old woman. Longitudinal endovaginal sonogram demonstrates regional bright echoes (arrow) with acoustic shadowing and diffuse low-level internal echoes. Both reviewers made the correct diagnosis.

 


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Figure 2. Hemorrhagic cyst of the right ovary in a 21-year-old woman. Transverse endovaginal sonogram reveals fibrinous strands (arrow) and low-level internal echoes. The margins of the ovary are marked with electronic cursors (+, x). Both reviewers made the correct diagnosis.

 


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Figure 9. Benign left ovarian neoplasm in a 38-year-old woman. Longitudinal endovaginal sonogram demonstrates low-level echoes and foci of mural nodularity (arrows). This was diagnosed as a neoplasm, type unspecified, by both reviewers.

 


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Figure 4. Endometrioma in a 28-year-old woman. This lesion exhibits diffuse low-level internal echoes and punctate peripheral echogenic foci (arrows) on this oblique endovaginal sonogram. Both reviewers made the correct diagnosis.

 


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Figure 5. Detailed view of an endometrioma in a 33-year-old woman. Hyperechoic wall foci (arrow) and low-level echoes are shown on this longitudinal endovaginal sonogram. Both reviewers made the correct diagnosis.

 


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Figure 6. Multiloculated endometrioma in a 40-year-old woman. Oblique transabdominal sonogram demonstrates a cystic adnexal mass with internal septations (arrow). Low-level echoes are seen within portions of this lesion. One reviewer diagnosed a benign neoplasm, and the other did not offer a specific diagnosis.

 


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Figure 7. Endometrioma of the right ovary in a 42-year-old woman. The lesion is marked by electronic cursors (+ and x). Diffuse low-level echoes and focal wall nodularity (arrow) are shown on this transverse endovaginal sonogram. Both reviewers diagnosed neoplasm, type unspecified.

 
On the basis of the overall US appearance of a mass, each reviewer independently chose one specific conclusion from a list of possibilities, with emphasis on achieving the highest positive predictive value for any particular diagnosis. The specific diagnoses that could be made were as follows: (a) endometrioma; (b) dermoid; (c) hemorrhagic cyst; (d) nonhemorrhagic, nonneoplastic cyst; (e) benign neoplasm; (f) malignant neoplasm; (g) neoplasm, uncertain whether benign or malignant; (h) other (specify); and (i) no specific diagnosis.

The sensitivity, specificity, positive predictive value, negative predictive value, negative likelihood ratio, and positive likelihood ratio were analyzed for the diagnosis of endometrioma according to each US finding and selected combinations of findings. It should be recognized that the sensitivity analysis reflects the ability of any particular set of findings or any individual reviewer to identify ultrasonographically detected endometriomas. Our study design does not allow for determination of the true sensitivity of disease detection because patients without ultrasonographically identified adnexal masses were not surgically evaluated. The negative likelihood ratio is defined as (1 - sensitivity)/specificity, and the positive likelihood ratio is defined as sensitivity/(1 - specificity). Likelihood ratios have surfaced in the medical decision-making literature as a method to describe the change in odds favoring disease given a particular test result (11). When a likelihood ratio exceeds 1, the odds favoring disease increase; when the likelihood ratio becomes less than 1, the odds favoring disease decrease. Likelihood ratios are useful because they do not change with the pretest probability of disease, unlike sensitivity and specificity. The receiver operating characteristic curve with the highest diagnostic performance established by using this analysis was generated.


    RESULTS
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Among the 252 masses, there were 40 endometriomas (16% prevalence). Of the 212 nonendometriomas, there were 74 cystic teratomas, 49 benign neoplasms, 18 malignant neoplasms, 30 hemorrhagic cysts, 39 other nonneoplastic cysts (16 histopathologically proved nonneoplastic ovarian cysts, 17 self-resolving anechoic ovarian cysts, four cases of hydrosalpinx, and two paratubal cysts), one case of ovarian torsion, and one broad ligament myoma. Table 1 lists the sensitivity, specificity, positive predictive value, negative predictive value, positive likelihood ratio, and negative likelihood ratio for the prediction that an adnexal mass is an endometrioma for each US feature and selected combination of features and for each reviewer. Figure 10 is the highest receiver operating characteristic curve generated by using these data, with the performance of each reviewer superimposed. Table 2 compares the positive likelihood ratios of selected combinations of findings before and after the performance of follow-up US to exclude spontaneously resolving hemorrhagic cyst as a diagnostic possibility.


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TABLE 1. Diagnostic Performance of US Features and Reviewers in Discriminating between Endometriomas and Nonendometriomas
 


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Figure 10. Highest receiver operating characteristic curve for diagnosis of endometrioma by using the US features evaluated in this study (-). The performances of reviewer 1 (+) and reviewer 2 (x) are superimposed.

 

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TABLE 2. Positive Likelihood Ratios of US Features before and after Exclusion of Spontaneously Resolving Lesions at Follow-Up US
 

    DISCUSSION
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
The broad range in US appearance that endometriomas can manifest has been well publicized (1,12,13). This, unfortunately, leads to the mistaken impression that it is impossible to achieve a high positive predictive value in the US diagnosis of endometrioma. Several investigators have sought to identify the diagnostic performance of US in distinguishing endometriomas from other adnexal masses, with each group using features different than those used by the others. Three investigations from the University of Cagliari, Italy, evaluated 82, 101, and 118 masses (of which 25, 29, and 39 were endometriomas) that had a positive likelihood ratio of 8.0–35.1 and a negative likelihood ratio of 0.2 for the diagnosis of endometrioma by using the US criteria of "round, intraovarian, homogeneous, hypoechoic tissue, with a clear demarcation from the parenchyma and without papillary proliferations" (35). Using the criteria "diffuse homogeneously dispersed low-level echoes within a well-marginated thin cystic mass" to discriminate seven endometriomas from 43 other masses, Jain (6) had a positive likelihood ratio exceeding 37 and a negative likelihood ratio of 0.1. Volpi et al (7), evaluating 180 adnexal masses, of which 57 were endometriomas, searched for "a cystic structure with low, homogeneous echogenicity and a thick cystic wall . . . with regular margins" but not excluding "very fine papillary structures, not exceeding 3 mm" and had a positive likelihood ratio of 33.8 and a negative likelihood ratio of 0.2. Most recently, Alcazar and colleagues (8) found a positive likelihood ratio of 9.8 and a negative likelihood ratio of 0.1 in distinguishing 27 endometriomas from 55 other adnexal masses by using "the presence of a round-shaped homogeneous hypoechoic mass of low-level echoes" as the diagnostic criteria.

Clearly, there is a range in what experts have defined as a "classic" endometrioma. These studies have not addressed which of the criteria used are most important in discriminating between an endometrioma and other adnexal lesions. While the presence of low-level echoes is a uniform diagnostic criterion for all studies, diagnostic requirements for the thickness and contour of the wall and shape and location of the lesion differ among the investigations. Understanding the degree to which any particular feature or set of features increases or decreases the likelihood ratio for the diagnosis of endometrioma is important, because one can then use this knowledge to direct the evaluation toward identifying those features that have the greatest relevance and avoid effort and confusion in characterizing those features that have no relevance.

Our study systematically addressed these issues, and our findings confirm that the presence of diffuse low-level internal echoes is the important feature that helps to discriminate an endometrioma from other lesions; 95% of endometriomas exhibit diffuse low-level internal echoes (Figs 48). While the absence of this finding does not exclude endometrioma, it significantly decreases the likelihood of that diagnosis (negative likelihood ratio, 0.1). It is interesting that cystic US features (definable wall and increased acoustic transmission) did not improve diagnostic performance once diffuse low-level echoes had been recognized.



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Figure 8. Endometrioma of the left ovary in a 29-year-old woman. Transverse endovaginal sonogram reveals diffuse low-level echoes and focal wall nodularity (arrow). Neither reviewer offered a specific diagnosis. The electronic marker denotes one of the focal zones.

 
Certain US features (focal acoustic impedance, regional bright echoes, and hyperechoic lines and dots) are predictive of cystic teratomas (Fig 1) (14). Because most endometriomas do not demonstrate these features, excluding masses with these features improves diagnostic performance; in our study, this strategy increased the positive likelihood ratio from 5 to 8, with a small decrease in sensitivity from 95% to 90%.

Our data suggest that there is no diagnostic value to the assessment of wall thickness. This feature had the greatest interobserver variability in our study, with disparate assignment of wall thickness in 36 (17%) of 210 masses considered to demonstrate cystic US features. While different groups of investigators have stipulated that one must demonstrate a thin wall (6) or thick wall (8) to confidently diagnose endometriomas, our data indicate that wall thickness is not a distinguishing criterion.

On the other hand, we demonstrate considerable benefit from the assessment of wall nodularity, a feature that is associated with neoplasia (15). Excluding masses with wall nodularity from the diagnosis of endometrioma helped to exclude neoplasm, especially malignancy, as a false-positive diagnosis (Fig 9). However, as eight (20%) of 40 endometriomas demonstrated wall nodularity, using the presence of wall nodularity as an exclusionary diagnostic criterion reduces the sensitivity of identifying endometriomas (Figs 7, 8). Altogether, there were 11 masses in our study that demonstrated low-level internal echoes with wall nodularity but no features of cystic teratoma, of which six were endometriomas and five were neoplasms. The subgroup of patients with these masses may benefit from additional imaging with color Doppler US, magnetic resonance (MR) imaging, or both to try to distinguish between neoplastic and nonneoplastic causes of wall nodularity.

Hemorrhagic ovarian cysts can also demonstrate diffuse low-level internal echoes (Figs 2, 3) and typically do not demonstrate those features discussed above that are associated with dermoids or other neoplasms (termed "neoplastic features" for the remainder of this discussion). Using only these criteria to predict that a mass is an endometrioma yields a positive likelihood ratio of 8, with the majority of false-positive diagnoses representing hemorrhagic cysts. Hemorrhagic cysts are almost exclusively nonneoplastic. Thus, they resolve spontaneously and are surgically removed only when patients have compelling acute symptoms. This has justifiably led to the practice of follow-up US as a diagnostic strategy to use when a mass is thought most likely to represent an endometrioma but that alternatively may represent an acutely hemorrhagic cyst, a strategy that virtually eliminates the possibility that a patient will undergo an unnecessary operation.



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Figure 3. Hemorrhagic cyst of the right ovary in a 38-year-old woman. Electronic cursors mark the lesion (x) and the ovary (+). This lesion was shown to have resolved on a subsequent sonogram obtained 6 months later. On this longitudinal endovaginal sonogram, diffuse low-level internal echoes are shown. One reviewer incorrectly diagnosed this mass as an endometrioma, and the other reviewer did not offer a specific diagnosis.

 
Our data document the usefulness of this strategy (Table 2). Hemorrhagic cysts are commonly discovered because intracyst hemorrhage is acutely symptomatic, whereas endometriomas, as persistent lesions, are seen only serendipitously with fresh hemorrhage. Fibrinous strands (Fig 2) and retracting clots are US findings that suggest recent hemorrhage (6). As indicated by our study findings, only three (8%) of 40 endometriomas demonstrate features associated with acute hemorrhage when studied ultrasonographically. Thus, using the presence of fibrinous strands and retracting clots as exclusionary diagnostic criteria improves the positive likelihood ratio of the US diagnosis of endometrioma, but not to a level obviating follow-up US if one strives to avoid all unnecessary surgeries.

Demonstration of hyperechoic wall foci in a mass with low-level echoes and absence of neoplastic features is strongly predictive of an endometrioma (Figs 4, 5). We separately evaluated "wall nodularity" from "hyperechoic wall foci." Thirty-five percent of endometriomas in our series demonstrated these foci, while only 6% of nonendometriomas did so. Hyperechoic wall foci yielded a positive likelihood ratio of 6.2, the highest positive likelihood ratio for a single feature in our study. This finding helps to distinguish endometriomas from nonneoplastic cysts. In our experience, hyperechoic wall foci were seen in only one of 69 nonneoplastic cysts (a mass that did not resolve with periodic US follow-up and that was considered a "simple" cyst at histopathologic analysis). Thus, our data indicate that a mass with low-level internal echoes, hyperechoic wall foci, and no neoplastic features is 32 times more likely to be an endometrioma than another adnexal mass and that US follow-up in such lesions is a low-yield course of action (Table 2).

To our knowledge, the pathologic basis of these hyperechoic wall foci has not been established. Given the similarity in appearance to hyperechoic wall foci seen in the gallbladder wall in patients with hyperplastic cholecystosis, due to the presence of cholesterol within polyps or Rokitansky-Aschoff sinuses, we postulate that these foci may contain cholesterol, perhaps from the breakdown of cell membranes. This may explain why they are seen in endometriomas, which contain chronic collections of cells that have had time to break down, and are not seen in spontaneously resolving lesions.

Another feature of diagnostic usefulness is the presence of septations without nodularity, also known as multilocularity. In our series, 18 of 40 endometriomas and 65 of 212 nonendometriomas were multilocular (Fig 6). However, when used as a feature in addition to low-level echoes and absence of neoplastic features, multilocularity increased the likelihood that a mass was an endometrioma. As a result, a mass with low-level echoes, without neoplastic features, and with multilocularity is 64 times more likely to represent an endometrioma than another adnexal mass. Follow-up US for masses with these features is unlikely to alter management (Table 2).

The diagnostic performance of the two experienced reviewers in this study fell directly but at different points on the receiver operating characteristic curve generated by means of our data analysis (Fig 10). This observation suggests that the ability of experienced sonologists to recognize and diagnose endometriomas is based on the criteria presented and does not result from features untested in our analysis. It is important that in no patient was an ovarian malignancy misdiagnosed as an endometrioma, either by an individual reviewer or by using the diagnostic features to discriminate endometriomas from other lesions. One limitation of our study design is that three possibly pertinent features in the discrimination of endometriomas from other adnexal lesions, namely, lesion shape, size, and location, were not evaluated. This study analyzed adnexal masses that were not related to pelvic inflammatory disease or ectopic pregnancy. While these entities may manifest US features similar to those discussed here, the clinical presentations in patients with pelvic inflammatory disease and ectopic pregnancy differ.

In conclusion, our data demonstrate that gray-scale US can achieve a high degree of accuracy in the diagnosis of endometrioma. An adnexal mass with diffuse low-level internal echoes and absence of particular neoplastic features is highly likely to be an endometrioma if there are no features of acute hemorrhage and especially if multilocularity or hyperechoic wall foci are present. In addition, our data indicate that a diagnosis of endometrioma is highly unlikely when no component of an adnexal mass contains low-level internal echoes. These data help to define the subgroup of patients with suspected endometriomas who may benefit from further diagnostic testing. For those masses with low-level internal echoes, follow-up US appears most useful when the mass has no wall nodularity, is unilocular, and does not possess hyperechoic wall foci, while MR imaging may be useful in discriminating between endometriomas and neoplasms when wall nodularity is present.


    Footnotes
 
Address reprint requests to M.D.P., Department of Radiology, Mayo Clinic Scottsdale, 13400 E Shea Blvd, Scottsdale, AZ 85259.

Author contributions: Guarantors of integrity of entire study, M.D.P., R.A.F.; study concepts, M.D.P., V.A.F., R.A.F.; study design, M.D.P.; definition of intellectual content, M.D.P., V.A.F., R.A.F.; literature research, M.D.P., D.C.C.; data acquisition, M.D.P., V.A.F., D.C.C., S.D.L., R.A.F.; data analysis, M.D.P., R.A.F.; statistical analysis, M.D.P.; manuscript preparation, M.D.P., V.A.F., R.A.F.; manuscript editing, M.D.P., R.A.F.; manuscript review, M.D.P., V.A.F., R.A.F.

Received June 18, 1998; revision requested July 28, 1998; revision received August 25, 1998; accepted October 7, 1998.
    References
 TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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  3. Mais V, Guerriero S, Ajossa S, Angiolucci M, Paoletti AM, Melis GB. The efficiency of transvaginal ultrasonography in the diagnosis of endometrioma. Fertil Steril 1993; 60:776-780.[Medline]
  4. Guerriero S, Mais V, Ajossa S, Paoletti AM, Angiolucci M, Melis GB. Transvaginal ultrasonography combined with CA-125 plasma levels in the diagnosis of endometrioma. Fertil Steril 1996; 65:293-298.[Medline]
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  6. Jain KA. Prospective evaluation of adnexal masses with endovaginal gray-scale and duplex and color Doppler US: correlation with pathologic findings. Radiology 1994; 191:63-67.[Abstract/Free Full Text]
  7. Volpi E, De Grandis T, Zuccaro G, La Vista A, Sismondi P. Role of transvaginal sonography in the detection of endometriomata. J Clin Ultrasound 1995; 23:163-167.[Medline]
  8. Alcazar JL, Laparte C, Jurado M, Lopez-Garcia G. The role of transvaginal ultrasonography combined with color velocity imaging and pulsed Doppler in the diagnosis of endometrioma. Fertil Steril 1997; 67:487-491.[Medline]
  9. Outwater E, Schiebler ML, Owen RS, Schnall MD. Characterization of hemorrhagic adnexal lesions with MR imaging: blinded reader study. Radiology 1993; 186:489-494.[Abstract/Free Full Text]
  10. Takahashi K, Okada S, Okada M, Kitao M, Kaji Y, Sugimura K. Magnetic resonance imaging and serum CA-125 in evaluating patients with endometriomas prior to medical therapy. Fertil Steril 1996; 65:288-292.[Medline]
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  12. Atri M, Nazarnia S, Bret PM, Aldis AE, Kintzen G, Reinhold C. Endovaginal sonographic appearance of benign ovarian masses. RadioGraphics 1994; 14:747-760.[Abstract]
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  15. Sassone AM, Timor-Tritsch IE, Artner A, Westhoff C, Warren WB. Transvaginal sonographic characterization of ovarian disease: evaluation of a new scoring system to predict ovarian malignancy. Obstet Gynecol 1991; 78:70-76.[Abstract/Free Full Text]



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