(Radiographics. 2001;21:193-216.)
© RSNA, 2001
Endometriosis: Radiologic-Pathologic Correlation1
Paula J. Woodward, MD,
Roya Sohaey, MD and
Thomas P. Mezzetti, Jr, LCDR, USNR, MC
1 From the Departments of Radiologic Pathology (P.J.W.) and Gynecologic and Breast Pathology (T.P.M.), Armed Forces Institute of Pathology, Bldg 54, Room M-121, Washington, DC 20306-6000; the Department of Radiology, Oregon Health Sciences University, Portland (R.S.); and the Department of Radiology, University of Utah, Salt Lake City (P.J.W.). Received July 7, 2000; revision requested July 24; revision received August 1; accepted August 3. Address correspondence to P.J.W. (e-mail: woodwardp@afip.osd.mil).
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Abstract
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Endometriosis is an important gynecologic disorder primarily affecting women during their reproductive years. Pathologically, it is the result of functional endometrium located outside the uterus. It may vary from microscopic endometriotic implants to large cysts (endometriomas). The physical manifestations are protean, with some patients being asymptomatic and others having disabling pelvic pain, infertility, or adnexal masses. Symptoms do not necessarily correlate with the severity of the disease. Ultrasonographic (US) features are variable and can mimic those of other benign and malignant ovarian lesions. Low-level internal echoes and echogenic wall foci are more specific US features for endometriomas. Magnetic resonance imaging improves diagnostic accuracy, with endometriotic cysts typically appearing with high signal intensity on T1-weighted images and demonstrating "shading" on T2-weighted images. The ovaries are the most common sites affected, but endometriosis can also involve the gastrointestinal tract, urinary tract, chest, and soft tissues. Small implants and adhesions are not well evaluated radiologically; therefore, laparoscopy remains the standard of reference for diagnosis and staging. Both medical and surgical treatment options are available depending on the patient's specific case.
Index Terms: Endometriosis, 70.318, 80.3192
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LEARNING OBJECTIVES FOR TEST 5
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After reading this article and taking the test, the reader will be able to:
- Outline the proposed mechanisms of pathogenesis of endometriosis and how they relate to the distribution of disease.
- Identify which imaging features are more specific for endometriosis and help to distinguish it from other adnexal masses.
- Describe the unusual manifestations and complications that can be seen with endometriosis.
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Introduction
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Endometriosis is classically defined as the presence of functional endometrial glands and stroma outside the uterine cavity (ectopic as opposed to normally located or eutopic endometrium). In older literature, endometriosis was further classified as endometriosis interna and endometriosis externa. Endometriosis interna referred to endometrial tissue within the uterine musculature, and endometriosis externa referred to endometrial tissue in all other sites. Currently, the term adenomyosis has replaced endometriosis interna. Adenomyosis is considered a distinct and different clinical entity because its pathogenesis, symptoms, and epidemiology differ from those of endometriosis. Endometriosis externa is now simply called endometriosis and is the condition reviewed in this article.
Endometriosis is a common and important clinical problem of women, predominantly those in the reproductive age group. At pathologic analysis, it can vary from microscopic foci to large, grossly visible endometriotic cysts (endometriomas). Radiologists are often involved in the diagnosis and work-up of this disease in one of two scenarios: They are asked to exclude endometriosis in a woman with pelvic pain or infertility or they are considering endometriosis in the differential diagnosis of an adnexal mass.
Radiologists often use the terms endometriosis and endometriomas interchangeably. It is important to remember, however, that endometriomas are only a part of the disease process, which also includes endometriotic implants and adhesions. All of these features are important in the staging of endometriosis, and normal results from an imaging procedure do not rule out the presence of disease.
To help radiologists better understand this disease process, we review its epidemiology, pathogenesis, staging, and clinical features. Although its imaging characteristics overlap with those of other adnexal masses, those features more specific to endometriosis are discussed, along with the strengths and weaknesses of the various imaging modalities. Endometriosis can also occur in nongynecologic sites. A knowledge of these locations, their clinical manifestations, and radiologic appearances will aid radiologists in considering endometriosis in the differential diagnosis. Atypical manifestations of endometriosis, complications, and treatment are also discussed.
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Epidemiology
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Endometriosis is found predominantly in women of childbearing age. The mean age at diagnosis is 25–29 years, but it is often greater in women who present with infertility rather than pelvic pain (1). Endometriosis is not uncommon among adolescents. Approximately half of women under 20 years of age who have chronic pelvic pain or dyspareunia have the disease (2,3). Obstructive müllerian duct anomalies of the cervix or vagina account for most cases of endometriosis in girls under the age of 17 years (4). About 5% of endometriosis cases are seen in postmenopausal women, and exogenous estrogen replacement therapy is suggested to play a role (5). In rare cases, men undergoing long-term estrogen therapy may be affected (5).
The prevalence of endometriosis is difficult to determine accurately. Laparoscopy or surgery is required for the definitive diagnosis. Endometriosis has been reported in 4.1% of asymptomatic women undergoing laparoscopy for tubal ligation. However, in the same study, 20% of women undergoing laparoscopic investigation for infertility and 24% of women with pelvic pain had endometriosis (6). Overall prevalence, including both symptomatic and asymptomatic women, is estimated to be 5%–10% (7,8).
When social and economic factors are accounted for, the prevalence of endometriosis is the same in women of different races (9,10). In a recent study, investigators compared menstrual characteristics that would increase peritoneal exposure to menstrual fluid with the risk of developing endometriosis. The three characteristics studied were age of menarche, duration of menstrual flow, and menstrual cycle length. The only menstrual characteristic that was significantly associated with endometriosis was a menstrual cycle length of less than 28 days (11). An increased prevalence of endometriosis in families has been observed, and therefore a genetic effect has been suggested (12).
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Pathogenesis
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Endometriosis is a complex disorder, and its causes are probably multifactorial. Three theories of histogenesis have been proposed: (a) metastatic theory (retrograde menstrual implantation, vascular and lymphatic spread, and intraoperative implantation), (b) metaplastic theory, and (c) induction theory (Fig 1). In addition, researchers are presently investigating the role of growth factors, immunity, and other mechanisms that may contribute to the development of this disorder.
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Figure 1. Drawing depicts the potential mechanisms of endometriosis pathogenesis, including retrograde menstruation (a), lymphatic spread (b), hematogenous spread (c), and coelomic metaplasia (d). Induction of undifferentiated mesenchyma by unidentified endometrial substances is also theorized.
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The most widely accepted theory is that endometriosis results from metastatic implantation from retrograde menstruation (7,13,14). The theory assumes transportation of endometrial tissue from the uterus in a retrograde fashion into the peritoneal cavity. The endometrial cells remain viable and implant on serosal surfaces outside the uterus. The occurrence of retrograde menstruation has been documented with diagnostic laparoscopy and studies of peritoneal dialysis fluid. Up to 90% of women have bloody peritoneal fluid during the perimenstrual period (15–17). Investigators have shown the in vitro growth potential of shed endometrium and have demonstrated viable endometrial cells in peritoneal fluid (7,18,19). Further evidence for this theory is suggested by the anatomic pattern of the disease within the dependent areas of the pelvis (Fig 2) (20). Endometriosis is also seen with greater frequency in women with excessive retrograde flow due to obstructive anomalies of müllerian duct development (21). Other possible routes of metastatic spread include transport of endometrial cells to distant sites via the blood stream or lymphatic channels or iatrogenically during surgery or needle biopsy (22).
A second theory of histogenesis is that of metaplastic differentiation of serosal surfaces (coelomic epithelium) or müllerian remnant tissue. Both endometrial and peritoneal cells derive from the coelomic wallepithelium. The theory suggests the possibility of peritoneal cells differentiating into functioning endometrial cells. The strongest evidence for this theory is the demonstration of endometriosis in women lacking functional eutopic endometrium (eg, those with Turner syndrome, gonadal dysgenesis, uterine agenesis) and in men (22). In the rare cases of endometriosis occurring in men, they have usually received high doses of estrogen, which is sometimes done in the treatment of prostate carcinoma (7,23,24). In these men, the cause is possibly hyperplasia and spread of endometrial tissue from the prostatic utricle (a müllerian remnant) (7).
A third theory, the induction theory of endometriosis, is a combination of the first two. It suggests that shed endometrium releases substances that induce undifferentiated mesenchyma to form endometriotic tissue (7). These substances have not been identified, but animal research has shown the formation of endometrial glands (but not stroma) when experiments have been performed to test this theory (7,25).
Regardless of which theory is correct, other factors probably play a role in the occurrence of endometriosis, since all women are not equally susceptible. Impairment of the immune response to remove peritoneal menstrual debris has been suggested as an additional factor. Women with endometriosis have been found to have abnormalities of T-cell–mediated cytotoxicity, natural killer cell activity, B-cell function, and complement deposition (26,27). The role of growth factors and factors critical to cell implantation are also receiving attention (7).
Finally, the biologic behavior of ectopic endometrial glands is variable and adds to the complexity of the disease. Ectopic endometriotic implants generally respond to circulating hormones in the same manner as eutopic endometrium (though to a lesser degree). Estrogen stimulates glandular growth, whereas progesterone inhibits it. However, ectopic endometrium often behaves unpredictably, which leads to difficulties in diagnosis and treatment (22).
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Pathologic Features
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Gross pathologic findings of endometriosis depend on the duration of the disease and depth of penetration of the lesions. Endometriotic implants vary from punctate foci to small stellate patches (usually less than 2 cm). The amount of pigment in the implant appears to increase with the age of the lesion. They may initially be unpigmented or appear as white, yellow, or red foci, which progress to a more mature-appearing blue or brown lesion (Figs 3, 4) (22,28). These brown, ecchymotic areas have been described as "powder burns." Implants may change in appearance during the menstrual cycle, becoming more swollen and congested during menses and bleeding in some cases. These mature endometriotic foci initiate an inflammatory response, with areas of organizing hemorrhage, fibrosis, and adhesion formation. Extensive adhesions can distort the normal pelvic anatomy and obliterate the pouch of Douglas (22,28–30). The most common site of involvement is the ovary, but virtually all pelvic organs can be affected by the disease (Table 1) (20).
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Figure 4. Intraoperative view shows the surgeon retracting the uterus to reveal three dark-brown endometriotic implants in the cul-de-sac (arrows). These lesions are mature endometriotic implants.
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Endometriotic cysts (endometriomas) generally occur within the ovaries and are the result of repeated cyclic hemorrhage within a deep implant. They may completely replace normal ovarian tissue. Cyst walls are generally thick and fibrotic and commonly have areas of discoloration and dense fibrous adhesions. The cyst lining can vary from smooth and pale to shaggy and brown (Fig 5). Although cyst contents can be watery, they more typically are composed of thick, dark, degenerated blood products. This appearance has been called "chocolate cyst" (Fig 6). Endometriomas are bilateral in up to half of the cases and may be large, although they seldom exceed 15 cm in diameter (22,29). Large lesions and lesions with wall nodularity should be carefully sampled to rule out malignancy.
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Figure 5a. Left ovarian endometrioma in a 30-year-old woman. (a) Transabdominal US scan shows a hypoechoic mass replacing the left ovary (arrows). Note the thickened wall. (b) Photograph of the gross specimen (external surface on the left and internal surface on the right) reveals stellate patches of hemorrhage on the external surface (solid arrows) and a thick-walled, dark, irregular internal cyst lining. A portion of the fallopian tube was adherent to the endometrioma (open arrow). Scale is in centimeters.
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Figure 5b. Left ovarian endometrioma in a 30-year-old woman. (a) Transabdominal US scan shows a hypoechoic mass replacing the left ovary (arrows). Note the thickened wall. (b) Photograph of the gross specimen (external surface on the left and internal surface on the right) reveals stellate patches of hemorrhage on the external surface (solid arrows) and a thick-walled, dark, irregular internal cyst lining. A portion of the fallopian tube was adherent to the endometrioma (open arrow). Scale is in centimeters.
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Figure 6a. Right ovarian endometrioma in a 25-year-old woman. (a) Transvaginal US scan shows an echogenic ovarian cyst filled with low-level echoes. (b) Photograph of the resected cyst, which has been opened, shows dark-brown, viscous blood products. This appearance has been called a chocolate cyst. Multiple irregular hemorrhagic foci are seen on the external surface of the cyst.
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Figure 6b. Right ovarian endometrioma in a 25-year-old woman. (a) Transvaginal US scan shows an echogenic ovarian cyst filled with low-level echoes. (b) Photograph of the resected cyst, which has been opened, shows dark-brown, viscous blood products. This appearance has been called a chocolate cyst. Multiple irregular hemorrhagic foci are seen on the external surface of the cyst.
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At microscopic analysis, endometriosis is composed of endometrial glands, stroma, and occasionally smooth muscle fibers. As with eutopic endometrium, the ectopic endometrial foci respond to circulating hormones and may show secretory changes during the second half of the menstrual cycle and stromal decidualization during pregnancy (28). Hemorrhage within these foci results in an inflammatory response, with infiltration of histiocytes that become pigment laden with hemosiderin and hemofuscin (Fig 7) (22,30). In rare cases, endometriosis may lack glands (stromal endometriosis) (22).
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Figure 7a. Microscopic appearance of an endometriotic implant. (a) Medium-power photomicrograph (original magnification, x4; hematoxylin-eosin stain) shows endometriotic glands and stroma (center). The endometriotic tissue is surrounded by fibrosis (arrows) as well as degraded blood products and inflammatory debris (*). (b) High-power photomicrograph (original magnification, x80; hematoxylin-eosin stain) shows dark-brown particles of hemosiderin or hemofuscin (straight arrows) and scattered red blood cells (curved arrows). A layer of endometriotic glands is partially visible in the lower left corner.
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Figure 7b. Microscopic appearance of an endometriotic implant. (a) Medium-power photomicrograph (original magnification, x4; hematoxylin-eosin stain) shows endometriotic glands and stroma (center). The endometriotic tissue is surrounded by fibrosis (arrows) as well as degraded blood products and inflammatory debris (*). (b) High-power photomicrograph (original magnification, x80; hematoxylin-eosin stain) shows dark-brown particles of hemosiderin or hemofuscin (straight arrows) and scattered red blood cells (curved arrows). A layer of endometriotic glands is partially visible in the lower left corner.
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Clinical Characteristics
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Symptoms associated with endometriosis include infertility and pelvic pain. These nonspecific symptoms can accompany a wide variety of disorders and are not pathognomonic for endometriosis. Unusual symptoms linked to atypical location of disease can also occur. The extent of endometriosis does not always correlate with the severity of symptoms, which further complicates the diagnosis. However, endometriosis should be considered in any woman of reproductive age with pelvic pain or infertility.
Infertility, with or without pelvic pain, may be the presenting complaint in women with endometriosis. It is estimated that 30%–50% of women with endometriosis are infertile, and 20% of infertile women have endometriosis (6,31). Although the association between the two is well established, the causal mechanism is debated. An acceptable explanation is that endometriomas and adhesions cause pelvic distortion, which leads to impaired ability of the fallopian tubes to capture ovum (7,31). In cases in which minimal endometriosis is present, the clinician must decide if the finding is incidental. Some proposed mechanisms for infertility in women with minimal disease include abnormalities related to autoimmunity and peritoneal fluid factors (31).
Pelvic pain is a frequent complaint from women with endometriosis. Common symptoms include dysmenorrhea, dyspareunia, chronic pelvic pain, back pain, and rectal discomfort (8). The pain is not always cyclic, and endometriosis is present in approximately one-third of patients with chronic pelvic pain (31).
Unusual symptoms may occur when endometriotic implants occur in atypical locations. Involvement of the gastrointestinal tract may manifest with catamenial diarrhea, rectal bleeding, and constipation. Bladder involvement may result in urgency, frequent urination, and hematuria. Ureteral involvement may cause urinary obstruction and flank pain. Pleuritic chest pain, pneumothorax, pleural effusions, or cyclic hemoptysis can occur with pulmonary involvement (32). Cyclic headaches, seizures, and subarachnoid hemorrhage have been described with brain lesions (33,34). Cutaneous lesions may manifest with catamenial bleeding and tenderness (31).
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Diagnostic Evaluation: Physical Examination, Laparoscopy, and Staging
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Physical findings for endometriosis are nonspecific. Localized tenderness along the uterosacral ligaments and the cul-de-sac is often present. Thickened or nodular ligamental or rectovaginal masses may be palpated. Adnexal tenderness or masses may be found if there is ovarian involvement. Pelvic organs may be fixed from adhesions, with the uterus often fixed in a retroverted position (7). The physical examination should be performed during early menses because implants are more likely to be large and tender at this time in the cycle. However, most women with endometriosis have normal or nonspecific results from physical examinations, and laparoscopy is necessary for the definitive diagnosis (13).
Laparoscopy is the standard of reference in the diagnosis of endometriosis. Although histologic analysis of biopsy specimens to confirm the diagnosis is desirable, it is not necessary. Staging of the disease can also be done during laparoscopy. Endometriotic implants, endometriomas, and adhesions are the typical findings. Implants may measure from a few millimeters to a few centimeters and may be superficial or deep. Because endometriotic implants can vary in appearance, the accuracy of diagnosis depends on the ability of the surgeon to recognize the disease (Figs 3, 4) (8). A pattern of lesion maturity has also been described, with subtle findings seen in young women and more characteristic features identified in the same women a decade later (35). Endometriotic cysts may be seen, most commonly involving the ovaries. Inflammatory response to active endometrial lesions can lead to fibrosis and adhesions. Severe adhesions may actually compartmentalize the pelvis and impede laparoscopic evaluation.
The most widely used staging system for endometriosis is the 1985 Revised Classification of Endometriosis published by the American Fertility Society (8,36). This system consists of three components: evaluation of the endometrial implants (location, size, and depth of penetration), degree of cul-de-sac obliteration, and evaluation of adhesions (amount of surface area involvement and appearance) (Table 2). On the basis of their score, patients are categorized as having minimal, mild, moderate, or severe disease. Critics of staging note that the stage of disease does not necessarily correlate with the severity of symptoms (7,13), and consistent treatment options based on stage of disease have not been established (7). Despite these limitations, staging is thought to offer some standardization in stratifying disease severity and in assessing response to therapy.
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Radiologic Evaluation of Endometriosis
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Not unexpectedly, radiologic evaluation of small endometriotic implants is limited; therefore, the radiologist's role is generally to identify and evaluate endometriotic cysts. Because symptoms are variable, patients may be referred for a diverse array of imaging studies, including excretory urography, barium studies, and computed tomography (CT). These techniques lack both sensitivity and specificity, and a variety of nonspecific radiologic findings may be seen. Ultrasonography (US) is the most common imaging modality used to evaluate suspected endometriosis. However, it is applicable only to the evaluation of endometriotic cysts; detection of adhesions or implants with US is only anecdotal. Magnetic resonance (MR) imaging has proved to be a very useful and more specific imaging technique and is often used as a problem-solving tool.
Ultrasonography
Both transvesicular and transvaginal US should be performed. Cysts involving the ovaries should be completely characterized, with attention given to internal echogenicity, wall morphology, and effects on surrounding organs. Because the cul-de-sac is commonly involved, care should be taken during scanning to evaluate this area completely (Fig 8).
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Figure 8a. Diffuse endometriosis in a 27-year-old woman with pelvic pain. (a) Transabdominal midline sagittal US scan shows a complex cystic mass (white arrow) posterior to the uterus (U) filling the cul-de-sac (black arrow, right ovary). (b) Transvaginal US scan shows that the mass is contiguous with the serosal surface of the right ovary (arrow). (c) Photograph of the resected specimen shows extensive fibrous tissue and cysts filled with hemorrhage (arrows). This mass obliterated the cul-de-sac and was adherent to both the right ovary and appendix. Scale is in centimeters.
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Figure 8b. Diffuse endometriosis in a 27-year-old woman with pelvic pain. (a) Transabdominal midline sagittal US scan shows a complex cystic mass (white arrow) posterior to the uterus (U) filling the cul-de-sac (black arrow, right ovary). (b) Transvaginal US scan shows that the mass is contiguous with the serosal surface of the right ovary (arrow). (c) Photograph of the resected specimen shows extensive fibrous tissue and cysts filled with hemorrhage (arrows). This mass obliterated the cul-de-sac and was adherent to both the right ovary and appendix. Scale is in centimeters.
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Figure 8c. Diffuse endometriosis in a 27-year-old woman with pelvic pain. (a) Transabdominal midline sagittal US scan shows a complex cystic mass (white arrow) posterior to the uterus (U) filling the cul-de-sac (black arrow, right ovary). (b) Transvaginal US scan shows that the mass is contiguous with the serosal surface of the right ovary (arrow). (c) Photograph of the resected specimen shows extensive fibrous tissue and cysts filled with hemorrhage (arrows). This mass obliterated the cul-de-sac and was adherent to both the right ovary and appendix. Scale is in centimeters.
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Endometriomas can have a variety of US appearances. The majority exhibit diffuse low-level internal echoes, with the "classic" endometrioma being described as a homogeneous, hypoechoic focal lesion within the ovary (Figs 5, 6) (37–41). In one recent study of 40 endometrial cysts, 95% demonstrated this finding (37). In rare cases, they may be anechoic, mimicking a functional ovarian cyst.
Endometriomas may be unilocular or multilocular. A multilocular-appearing endometrioma may actually consist of multiple separate cysts. Thin or thick septations may be present between these loculi. One study showed that in the absence of wall nodularity and in the presence of diffuse low-level echoes, a multiloculated mass was 64 times more likely to be an endometrioma (Fig 9) (37). In the absence of these features, neoplasia cannot be excluded (Fig 10).
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Figure 9a. Endometrioma with thin septations in a 26-year-old woman. Sagittal (a) and transverse (b) transvaginal US images show a cystic mass posterior to the uterus in the cul-de-sac. It is filled with low-level internal echoes and has a thin septation within it (long arrow). Bright echogenic foci are seen within the cyst wall (short arrows).
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Figure 9b. Endometrioma with thin septations in a 26-year-old woman. Sagittal (a) and transverse (b) transvaginal US images show a cystic mass posterior to the uterus in the cul-de-sac. It is filled with low-level internal echoes and has a thin septation within it (long arrow). Bright echogenic foci are seen within the cyst wall (short arrows).
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Figure 10a. Endometrioma with thick septations in a 35-year-old woman. (a) Transvaginal US scan shows thick septations (arrow) with areas of wall irregularity (arrowhead). (b) Photograph of the gross specimen shows an irregular wall and septations (forceps). This appearance overlaps with that of a neoplasm. Scale is in centimeters.
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Figure 10b. Endometrioma with thick septations in a 35-year-old woman. (a) Transvaginal US scan shows thick septations (arrow) with areas of wall irregularity (arrowhead). (b) Photograph of the gross specimen shows an irregular wall and septations (forceps). This appearance overlaps with that of a neoplasm. Scale is in centimeters.
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The US appearance of the endometrial cyst wall can be variable but deserves special attention. Diffuse wall thickening, wall nodularity, and echogenic foci within the cyst wall have been observed (37,39). Patel et al (37) found no diagnostic value in the assessment of wall thickness for differentiating between endometriomas and other ovarian masses. In their study, 20% of endometriomas had solid-appearing wall nodularity, a feature that is classically associated with neoplasia (37).
Echogenic wall foci differ from wall nodularity and are an important discriminating feature. These deposits are more echogenic and smaller than true wall nodules (Figs 9, 11). If not carefully searched for, these deposits may be missed. In the study performed by Patel et al (37), 35% of endometriomas demonstrated hyperechoic wall foci, compared with 6% of nonendometriomas. The finding was the highest single predictor for endometrioma. Although the pathologic basis of these echogenic foci has not been established, it is postulated that they form as cholesterol deposits accumulate in the endometriotic cyst wall. The finding is reminiscent of cholesterol deposits in the wall of a gallbladder with adenomyomatosis (37,41).
Dermoid cysts, hemorrhagic cysts, and cystic neoplasms can all overlap in their US appearances with that of endometriomas and must be considered in the differential diagnosis. However, careful analysis of the US characteristics will help narrow the differential possibilities. Dermoid cysts typically have unique identifiers such as calcification, fat-fluid levels, and hyperechoic areas (Fig 12). An acute hemorrhagic cyst can sometimes be difficult to differentiate from an endometrioma (Fig 13). Patient history may be helpful, since the symptoms accompanying hemorrhagic cysts are often more acute than those that usually occur with endometriosis. Hemorrhagic cysts will evolve into more complex-appearing cysts, with clot retraction and fibrin stranding, and generally resolve in 4–6 weeks. Fibrin strands can mimic the septations seen in an endometrioma, but they are generally thinner and are weaker reflectors compared with true septations (41). If the lesion resolves on a follow-up examination, an endometrioma is effectively ruled out. In addition to the above characteristics, endometriomas are more often multiple or bilateral, compared with the other benign lesions (Fig 14). If the cyst has soft-tissue components, a neoplasm must be excluded.
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Figure 12. Dermoid cyst. Transvaginal US scan demonstrates a cystic mass with an area of low-level echoes that could be mistaken for an endometrioma. However, the lesion also has a well-defined area of increased echogenicity (arrow), a finding that makes a dermoid cyst the more likely diagnosis.
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Figure 13. Hemorrhagic cyst mimicking an endometrioma. Transvaginal US scan shows a hypoechoic cystic lesion in the left ovary. The patient had presented with acute pain, a symptom that makes the diagnosis of a hemorrhagic cyst more likely. A 6-week follow-up scan showed resolution.
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In summary, the US features of endometriomas are quite variable and sometimes mimic other benign and malignant ovarian lesions. Diffuse low-level internal echoes and echogenic wall foci are more classic features. Endometriotic cysts may have septations, thickened walls, and wall nodularity. Because of this wide variability, endometriomas are considered by many to be the most difficult adnexal lesion to diagnose confidently with US. Short-term follow-up US or MR imaging can often help with making the diagnosis.
MR Imaging
As suggested, the confident US differentiation of endometriotic cyst from other adnexal masses may be difficult at times. MR imaging has been shown to have greater specificity for the diagnosis of endometriomas than other noninvasive imaging techniques (42–44). It affords a larger field of view than US, and the effect of adhesions on surrounding anatomic structures is better depicted. Therefore, MR imaging can be a helpful adjunct for evaluation of adnexal masses.
If available, MR imaging should be performed using a dedicated pelvic coil. These external multicoil arrays provide a higher signal-to-noise ratio, which improves spatial resolution and enhances visualization of anatomic detail. Imaging planes can include all three standard projections (axial, sagittal, and coronal), with the sagittal plane being particularly useful for evaluating the cul-de-sac and rectum.
In addition to using routine T1-weighted and T2-weighted pulse sequences, a T1-weighted fat-suppressed sequence should always be performed. Fat suppression narrows the dynamic signal range, thereby accentuating differences in tissue signal. Endometriomas have a relatively homogeneous high signal intensity (similar to or greater than that of fat) on T1-weighted images. With the high signal intensity of surrounding fat removed, lesion conspicuity is improved. Use of this pulse sequence is important in the evaluation of endometriosis. It has been shown to improve the sensitivity of MR imaging in the detection of small lesions and to increase its specificity, since fat-containing lesions such as dermoids are eliminated from the differential diagnosis (45–49).
Administration of gadolinium-based contrast material is not particularly useful in the evaluation of endometriomas. When used, the cyst wall demonstrates a nonspecific, variable enhancement pattern that does not differentiate it from other benign and malignant processes (47,50). In addition, a false-positive diagnosis may be made when normally enhancing parametrium is misinterpreted as endometriotic foci (51). Use of gadolinium should be reserved for those cases in which there is a concern for ovarian carcinoma.
Lesions with degenerated blood products, including methemoglobin and concentrated protein, appear with high-signal-intensity areas on T1- and T2-weighted images. A common and important feature of an endometrioma is "shading" (ie, loss of signal within the lesion), which can be seen on T2-weighted images (42,46). This shading reflects the chronic nature of an endometrioma and helps differentiate it from other blood-containing lesions. Blood products within these cysts are the result of cyclic bleeding accumulating over months to years. These chronic lesions are very viscous, with extremely high concentrations of iron and protein. At these high concentrations, protein cross-linking can occur, with a consequent decrease in T2-relaxation time. All of these factors may contribute to shading (42,52–54).
Shading is present when a cyst that is hyperintense on a T1-weighted image becomes hypointense on a T2-weighted image. Although the T2-weighted image often shows mixed high and low signal intensity, findings can be quite variable. Shading can range from faint, dependent layering to complete signal void, reflecting the concentration of blood products (42,53) (Figs 15, 16). Hemosiderin-laden macrophages combined with the fibrous nature of the cyst wall give it a low-sig-nal-intensity appearance on both T1- and T2-weighted images.
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Figure 15a. Bilateral endometriomas in a 27-year-old woman. (a) Axial T1-weighted MR image shows bilateral high-signal-intensity adnexal masses (solid arrows). An intrauterine device is seen within the uterus (open arrow). (b) On a T1-weighted fat-suppressed image, these masses remain bright, a finding that effectively rules out a diagnosis of dermoid cyst. (c) T2-weighted image shows shading with mixed high and low signal intensity in both lesions (arrows). Open arrow = intrauterine device.
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Figure 15b. Bilateral endometriomas in a 27-year-old woman. (a) Axial T1-weighted MR image shows bilateral high-signal-intensity adnexal masses (solid arrows). An intrauterine device is seen within the uterus (open arrow). (b) On a T1-weighted fat-suppressed image, these masses remain bright, a finding that effectively rules out a diagnosis of dermoid cyst. (c) T2-weighted image shows shading with mixed high and low signal intensity in both lesions (arrows). Open arrow = intrauterine device.
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Figure 15c. Bilateral endometriomas in a 27-year-old woman. (a) Axial T1-weighted MR image shows bilateral high-signal-intensity adnexal masses (solid arrows). An intrauterine device is seen within the uterus (open arrow). (b) On a T1-weighted fat-suppressed image, these masses remain bright, a finding that effectively rules out a diagnosis of dermoid cyst. (c) T2-weighted image shows shading with mixed high and low signal intensity in both lesions (arrows). Open arrow = intrauterine device.
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Figure 16a. Bilateral endometriomas in a 46-year-old woman. (a) Axial T1-weighted MR image shows a unilocular high-signal-intensity mass on the right and a multilocular high-signal-intensity mass on the left (arrows). (b) T2-weighted image shows that the right-sided mass remains high in signal intensity (short arrow), whereas the one on the left shows shading with marked signal loss (long arrows). The variable appearance of these lesions is thought to reflect the concentration of blood products.
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Figure 16b. Bilateral endometriomas in a 46-year-old woman. (a) Axial T1-weighted MR image shows a unilocular high-signal-intensity mass on the right and a multilocular high-signal-intensity mass on the left (arrows). (b) T2-weighted image shows that the right-sided mass remains high in signal intensity (short arrow), whereas the one on the left shows shading with marked signal loss (long arrows). The variable appearance of these lesions is thought to reflect the concentration of blood products.
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Looking at both the multiplicity and signal intensity of lesions, Togashi et al (42) found that a "definitive" diagnosis of an endometrioma was made when a cyst was hyperintense on T1-weighted images and shading was observed on T2-weighted images. The diagnosis was also "definitive" when multiple hyperintense cysts were seen on T1-weighted images regardless of their signal intensity on T2-weighted images. In their study, MR imaging yielded an overall sensitivity, specificity, and accuracy of 90%, 98%, and 96%, respectively. Because these cysts contain blood products of different ages and concentrations, cyst appearance can be variable. Those lesions that are not hyperintense on T1-weighted images can be difficult to distinguish from other adnexal masses (42,55).
Other lesions that appear with high signal intensity on T1-weighted images include dermoids, mucinous cystic neoplasms, and hemorrhagic masses. Dermoids can be recognized and differentiated from endometriomas by the presence of chemical shift artifact and signal drop-out on the fat-suppression images. Mucinous lesions can have increased signal intensity on T1-weighted images, but the signal is considerably less intense than that of fat or blood (55). The most problematic lesions to differentiate are hemorrhagic corpus luteum cysts, whose MR imaging appearance can be similar to that of endometriomas. Hemorrhagic cysts are usually unilocular as opposed to endometriomas, which are frequently multilocular and bilateral. In addition, hemorrhagic cysts do not exhibit shading on T2-weighted images and will resolve with time (46). A follow-up examination (this can be done with US) can confirm the diagnosis. Ovarian carcinoma can occasionally have internal hemorrhage. Visualization of solid components, septations, and a size larger than expected for an endometrioma are features suggestive of malignancy.
Despite advances in technology, the diagnosis of small endometriotic implants remains elusive. Their signal intensity is quite variable. They may appear similar to normal endometrium (ie, low signal intensity on T1-weighted images and high signal intensity on T2-weighted images), be hypointense with all pulse sequences, or be hyperintense with all pulse sequences (Fig 17) (43,55,56). Implants can enhance with gadolinium; however, this characteristic is neither sensitive nor specific (47).
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Figure 17a. Endometriosis with an endometriotic cyst, implants, and adhesions. Axial T1-weighted (a) and T2-weighted (b) MR images show the ovaries located more posteriorly than normally seen. The left ovary is replaced by an endometrioma, which has low signal intensity on the T1-weighted image and which shows posterior dependent shading on the T2-weighted image (solid curved arrow). There is a large endometriotic implant on the surface of the right ovary, which has high signal intensity with both pulse sequences (open straight arrow). Other implants were present at laparoscopy that were not seen on MR images. Note the adhesion extending from the right ovary to the posterior pelvic wall (solid straight arrow in b), which is made conspicuous by fluid on either side. Open curved arrow = uterus.
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Figure 17b. Endometriosis with an endometriotic cyst, implants, and adhesions. Axial T1-weighted (a) and T2-weighted (b) MR images show the ovaries located more posteriorly than normally seen. The left ovary is replaced by an endometrioma, which has low signal intensity on the T1-weighted image and which shows posterior dependent shading on the T2-weighted image (solid curved arrow). There is a large endometriotic implant on the surface of the right ovary, which has high signal intensity with both pulse sequences (open straight arrow). Other implants were present at laparoscopy that were not seen on MR images. Note the adhesion extending from the right ovary to the posterior pelvic wall (solid straight arrow in b), which is made conspicuous by fluid on either side. Open curved arrow = uterus.
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Complications
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Adhesions are an extremely common and important complication of endometriosis, and an attempt should be made to exclude them radiologically. During a US examination, a modified "physical examination" can be performed. The sonographer can use the transvaginal probe and gentle external pressure to better examine the pelvic organs and to detect if they are mobile or fixed. Fixed pelvic organs (ie, a fixed retroverted uterus) are suggestive of adhesions and should be noted in the radiologic report. At MR imaging, adhesions may sometimes be identified as spiculated low-signal-intensity stranding that obscures organ interfaces. Posterior displacement of the uterus and ovaries, angulation of bowel loops, elevation of the posterior vaginal fornix, loculated fluid collections, and a hydrosalpinx are also findings that suggest the presence of adhesions (Figs 17, 18) (55). Unfortunately, the extent and severity of adhesions can be difficult to determine with imaging, and laparoscopy is required for definitive diagnosis.
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Figure 18. Adhesions from endometriosis. Sagittal T2-weighted MR image shows an elevated posterior vaginal fornix. Bowel loops are tethered to this same area (arrow). These findings are subtle but suggestive of adhesions. Endometriotic implants (not seen on the MR images) and adhesions were found at laparoscopy.
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Focal leaks with inflammation, fibrosis, and adhesion formation are characteristics of endometriosis, whereas acute cyst rupture is a relatively uncommon complication. It has been reported in pregnancy and likely occurs because of softening of the lesion from stromal decidualization combined with pressure from the expanding uterus (22). Patients with a ruptured cyst present with symptoms of an acute abdomen.
Malignant transformation is a well-described, although rare (<1% of cases), complication of endometriosis. Approximately 75% of these tumors arise from endometriosis of the ovary (22). Other less common sites include the rectovaginal septum, rectum, and sigmoid colon (57). Unopposed estrogen therapy may play a role in the development of such tumors (22,57). Endometrioid carcinoma is the most common malignant neoplasm arising from endometriosis (Figs 19, 20), followed by clear cell carcinoma (58,59). Even when direct transition from endometriosis is not visualized, there is a definite association of both of these tumors with coexistent endometriosis (22). Large lesions and those with solid components suggest malignancy and must be removed (Fig 21).
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Figure 19. Endometrioid carcinoma. Medium-power photomicrograph (original magnification, x32; hematoxylin-eosin stain) shows endometriotic glands (open arrows) and well-differentiated endometrioid carcinoma (solid arrows).
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Figure 20a. Bilateral endometrioid carcinomas in a 30-year-old woman with pelvic pain and a palpable mass. (a) Axial CT scan shows bilateral ovarian masses with large, enhancing solid components (arrows). (b) Photograph of the resected left ovary shows a large solid component, as well as blood within the cystic portion. Endometriosis and endometrioid carcinoma were found at histologic analysis.
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Abstract
LEARNING OBJECTIVES FOR TEST...
