Women s Imaging Clinical Observations Verma et al. Sonohysterography and MRI of denomyosis Women s Imaging Clinical Observations Sachit K. Verma 1 nna S. Lev-Toaff 1,2 Oksana H. altarowich 1 Diane ergin 1,3 Manisha Verma 1 Donald G. Mitchell 1 Verma SK, Lev-Toaff S, altarowich OH, ergin D, Verma M, Mitchell DG 1 Department of Radiology, Thomas Jefferson University Hospital, 111 S 10th St., 10 Main ldg., Philadelphia, P 19107. ddress correspondence to. S. Lev-Toaff (anna.lev-toaff@uphs.upenn.edu). 2 Department of Radiology, Hospital of the University of Pennsylvania, Philadelphia, P. 3 Present address: Department of Radiology, Galway University Hospital, Galway, Ireland. P < P WOMEN S IMGING Keywords: adenomyosis, MRI, myometrium, sonohysterography DOI:10.2214/JR.08.1405 Received June 17, 2008; accepted after revision November 24, 2008. JR 2009; 192:1112 1116 0361 803X/09/1924 1112 merican Roentgen Ray Society denomyosis: Sonohysterography with MRI Correlation OJECTIVE. The purpose of this study was to describe the sonohysterographic features of adenomyosis with MRI correlation. CONCLUSION. In this study, when the sonohysterographic findings suggested adenomyosis, MRI findings confirmed the diagnosis in 96% of cases. Myometrial cracks are, to our knowledge, a previously undescribed sonohysterographic sign of adenomyosis. denomyosis is a common benign disease of the uterus characterized by ectopic endometrial glands and stroma within the myometrium associated with surrounding smooth-muscle hypertrophy [1, 2]. Symptoms are variable and nonspecific. Patients may have no symptoms or have dysmenorrhea, menorrhagia, pelvic pain, an enlarged uterus, or a combination of these findings [2 4]. The definitive diagnosis of adenomyosis, especially when myomas are also present, is best accomplished with MRI [3, 5 9]. The imaging investigation frequently begins with transvaginal sonography (TVS); however, with TVS alone it may be difficult to differentiate myometrial or subendometrial lesions from endometrial lesions, both of which can cause abnormal bleeding [3]. ecause of limitations regarding visualization of the uterine musculature at the location of ectopic endometrial glands, diagnostic hysteroscopy alone is not sufficient for the diagnosis of adenomyosis. The hysteroscopic finding of a normal-appearing endometrial cavity does not rule out adenomyosis [5]. Furthermore, the presence of adenomyosis can obscure the endometrium at TVS and make exclusion of an endometrial lesion difficult (pseudoendometrial thickening). To make the important distinction between myometrial (adenomyosis and fibroids) and endometrial lesions, sonohysterography (SHG) may be performed. SHG is a simple, safe, and convenient technique that enhances the diagnostic potential of TVS and often obviates biopsy [7]. The sonographic findings of adenomyosis are well described [10, 11] and include heterogeneous myometrial echotexture, asymmetric thickening of the anterior or posterior wall of the myometrium, myometrial cysts, subendometrial echogenic linear striations, and poor definition of the endometrial myometrial junction. previously undescribed, to our knowledge, diagnostic feature of adenomyosis at SHG is visualization of elongated tracks of fluid extending from the endometrial cavity into the myometrium. This feature, which corresponds to the flame-shaped or classic lollipop diverticula identified at hysterosalpingography (Fig. 1), is difficult to identify with TVS because the uterine cavity is imaged in a collapsed state. Likewise, on pelvic MR images, these tracks, which appear as areas of high signal intensity on T2-weighted images, may not be appreciated unless they course in the plane of the image. To our knowledge, there has been no report describing the SHG finding of tracking of fluid from the endometrial cavity into myometrial cracks. The purposes of our study were to describe the SHG features of adenomyosis, to make an MRI correlation, and to illustrate this peculiar sonographic appearance in women referred for evaluation of menorrhagia, infertility, or abnormal TVS findings. Materials and Methods Subjects database search covering the period January 2004 January 2007 at our institution yielded the cases of 26 women (mean age, 45 years; age range, 25 64 years) who underwent SHG and MRI of the pelvis with images from either technique suggesting the presence of adenomyosis. Clinical data 1112 JR:192, pril 2009
Sonohysterography and MRI of denomyosis were collected by chart review. The indications for SHG included abnormal bleeding (n = 22), infertility (n = 3), and tamoxifen use accompanied by abnormal TVS findings (n = 1). Twenty-three of the 26 women (88%) had SHG findings suggestive of adenomyosis. In the other three women (12%), adenomyosis was identified at MRI performed after SHG. For 23 of the 26 patients (88%), MRI was performed to assess for adenomyosis. For the other three women (12%), MRI was performed for evaluation of an adnexal mass (n = 1) or endo metrial thickening (n = 2). The mean time between SHG and MRI was 6 months (range, 2 12 months). Sonohysterographic Technique The following technique was used for SHG. single hinged speculum was inserted into the vagina, and the cervix was cleansed with antiseptic solution. 5- or 7-French balloon-bearing catheter was flushed with sterile saline solution and placed into the lower uterine segment or cervical canal. The balloon was inflated with a minimal amount of sterile saline solution. The speculum was removed, and a covered vaginal ultrasound probe was inserted. If necessary, the position of the catheter or the volume of saline solution in the balloon was adjusted under TVS observation. pproximately 10 50 ml of sterile saline solution was instilled into the uterine cavity under continuous observation with TVS. Scanning was performed with a variety of commercially available ultrasound systems and 5.0- to 7.5-MHz vaginal probes. The balloon was deflated immediately before the end of the procedure. dditional saline solution was instilled while the catheter was slowly withdrawn during an evalu ation of the lower uterine segment and cervical canal. Only static images were included for image review during this retrospective study. SHG was performed by two senior attending radiologists with 20 25 years experience in pelvic sonography and 10 15 years experience in performing SHG and interpreting the images. MRI MRI was performed with a 1.5-T super conducting unit (Signa, GE Healthcare, or Intera, Philips Healthcare). Standard MRI of the female pelvis at our institution includes axial and coronal 2D fast spin-echo T2-weighted (TR/TE, 2,500 4,000/80 90) spoiled dual gradient-echo sequences, axial and coronal T1-weighted in- and out-of phase (120 200/2.3 and 4.6, 90 flip angle) sequences, and sagittal fast spin-echo T2-weighted fat-suppressed sequences performed with a pelvic or torso phased-array coil. Parameters for 2D images included a section thickness of 5 6 mm with an intersection gap of 0 1 mm; matrix size, 256 160 192; field of view, 20 24 cm 2 ; number of signals acquired, 1 or 2. Three-dimensional dynamic contrast-enhanced spoiled gradient-echo MR images were obtained with 4-mm section thickness in 2.5-mm increments with zero-fill interpolation; 4 6/2; flip angle, 10 15 ; matrix size, 256 160; number of signals acquired, 0.6 or 1; field of view, 20 24 cm 2. Twenty milliliters of gadopentetate dimeglumine (Magnevist, ayer Schering Pharma) was administered IV with a power injector at 2 ml/s followed by a 20-mL saline flush. For breath-hold dynamic imaging, the initial acquisition was made immediately after a saline flush and a second acquisition immediately thereafter. pproximately 3 5 minutes after contrast administration, sagittal images were obtained with a similar 3D technique or with contiguous 5-mm-thick fat-suppressed 2D singlesection technique (22/2; flip angle, 30 ; matrix size, 256 160; field of view, 24 cm 2 ; number of signals acquired, 1). Image Review Static SHG and MR images and reports were evaluated and compared retrospectively at a Webbased PCS (isite, Philips Healthcare) by two experienced radiologists with more than 3 and 20 years experience in abdominal imaging. ny discrepancies were resolved by consensus. These radiologists reviewed the images and suggested the diagnosis of adenomyosis on the basis of one or more of the following findings on SHG: asymmetric thickening and echotexture of the myometrium, fluid tracking from the endometrial cavity into myometrial cracks, myometrial cysts, appearance of air bubbles in the myometrium, and indistinct endometrial myometrial junction. MRI findings were used to confirm the diagnosis of Fig. 1 40-year-old woman (not in current patient series) with surgically proven adenomyosis. Hysterosalpingogram shows numerous large lollipop diverticula (arrows) with configuration similar to myometrial cracks in our series. adenomyosis if any one of the following three criteria was present: junctional zone thickness greater than 12 mm, junctional zone cysts, or indistinct junctional zone [10, 11]. The lesions were further classified as diffuse or focal. Results mong 23 women with SHG findings suggesting adenomyosis, the frequencies of individual findings were as follows: asymmetric myometrial thickening and heterogeneous echotexture (n = 14, 61%) (Fig. 2), tracking of fluid from the endometrial cavity into the myometrial cracks (n = 6, 26%) (Figs. 3 and 4), myometrial cysts (n = 6, 26%), indistinct endometrial myometrial junction (n = 5, 22%), bright reflectors presumably representing air in the myometrium appearing during saline injection at SHG (n = 3, 13%), and a combination of two or more findings (n = 9, 39%) (Fig. 5). Correlation of the imaging findings with the indication for SHG showed that all of the women with myometrial cracks (n = 6, 26%) had menorrhagia. MRI findings confirmed the presence of adenomyosis in 22 of 23 women (96%), either focal (n = 6) or diffuse (n = 16). In three of the 23 women, adenomyosis was suspected on SHG because of the appearance of focal bright reflectors, presumably air bubbles, during real-time TVS observation while saline solution was being injected for SHG. These focal bright reflectors were not present on the TVS images obtained before saline injection. The appearance of these focal reflectors suggested that air bubbles in the injected saline solution entered the myometrium because of the presence of patent endometrial glandular channels. Fig. 2 25-year-old woman with menorrhagia. Sagittal oblique sonohysterogram shows thickened posterior myometrium with heterogeneous echotexture (arrows) consistent with focal adenomyosis. JR:192, pril 2009 1113
Verma et al. In addition to the bright reflectors, signs suggestive of adenomyosis were heterogeneous myometrial echotexture and bulky uteri. In two of these three women (66%), MRI showed focal adenomyosis, but the location of the focal adenomyosis on MR images was not the same as the location of bright reflectors on SHG. In addition to focal adenomyosis, MRI also confirmed the presence of two small mural fibroids (Fig. 6). In the third woman, MRI did not show adenomyosis but did show a dominant mural fibroid. In addition to having the suggested SHG finding of adenomyosis, four of the women (17%) had distinct, well-circumscribed small homogeneous masses thought to be fibroids, and five of the women (21%) had an endometrial polyp. Fig. 3 36-year-old woman with infertility and uterus didelphys., Sagittal sonohysterogram through right horn shows irregular fluid-filled channel originating from fundal endometrium and extending into fundal myometrium nearly to serosal surface (arrows)., xial T2-weighted fast spin-echo MR image (TR/TE, 2,800/85) shows hyperintense myometrial crack (arrowheads) through myometrium nearly to serosa. C, xial T2-weighted fast spin-echo MR image (2,800/85) slightly inferior in relation to shows hyperintense fundal endometrial cavity (double arrows) not to be confused with myometrial crack (arrowheads). lso evident is medial focus of increased signal intensity (single arrow) within thickened junctional zone consistent with adenomyosis. Discussion denomyosis has been found in as many as 70% of hysterectomy specimens [3]. We suspected the presence of adenomyosis in 23 of 26 women (88%) in this study. MRI depicted adenomyosis in 22 of these 26 women, an SHG detection rate of 85%. This value compares with previous reported detection rates of 53% and 89% with TVS accompanied by MRI and histopathologic correlation [9, 10]. With MRI, which is an accurate noninvasive technique for diagnosing adenomyosis [9], the presence of adenomyosis was confirmed in 22 of 23 (96%) of our patients in whom the presence of adenomyosis was suspected at SHG. variety of sonographic features of adenomyosis have been reported [11], but we observed that SHG shows additional features, particularly in characterizing adenomyosis adjacent to the endometrial canal and communicating with the endometrial cavity. We believe that because our balloon catheter technique entails instillation of fluid into the uterine cavity under pressure, SHG is capable of depicting features of adenomyosis that may not be detectable when the uterine cavity is collapsed or is only minimally distended. Thus SHG may be more sensitive than TVS alone in depicting certain features of adenomyosis in women with abnormal uterine bleeding. To our knowledge, our study is the first to describe the presence of ill-defined areas of fluid intravasation extending from the uterine cavity into the myometrium. These fluid tracks likely represent direct invasion of bas- Fig. 4 40-year-old woman with infertility. and, Early () and late () filling phases of hysterosalpingogram obtained 7 months before sonohysterography shows irregular elongated diverticulum-like collection of contrast material (arrow) originating from fundal aspect of uterine cavity. C, Sagittal sonohysterogram shows irregular elongated crack (arrows) in fundal myometrium that originates from endometrial cavity. alloon of hysterosalpingographic catheter () is in uppermost aspect of endometrial cavity. C C 1114 JR:192, pril 2009
Sonohysterography and MRI of denomyosis Fig. 5 46-year-old woman with menorrhagia. Sagittal sonohysterogram shows gross thickening of anterior uterine wall, diffuse myometrial heterogeneity, and scattered avascular cystic spaces (arrows). al endometrium into the myometrium with patent glandular channels. This feature is uncommon and not documented in previously published studies to our knowledge. The exact mechanism of the appearance of myometrial cracks is not yet completely understood. We hypothesize that this finding is caused by dilated endometrial glands that communicate with the uterine cavity. dditional studies with careful imaging and pathologic correlation would be helpful for understanding this finding. We additionally speculate that our observation may be related to the use of balloonbearing catheters for SHG, which allows greater distention of the endometrial cavity. The slightly added pressure of distention may be all that is necessary to fill the tracks with fluid. The tracks become conspicuous as saline solution seeps through the myometrial cracks, resulting in depiction of the cracks at SHG, as in 26% of our cases. It is uncertain whether these myometrial cracks can be observed without the instillation of fluid. lthough we suspect that the cracks may appear as an indistinct endometrial myometrial interface on TVS, pseudoendometrial thickening, or small irregularly shaped myometrial cysts, confirmation requires further study by careful comparison of the appearances of the subendometrial zone before and after saline instillation. The SHG myometrial cracks sign was also seen in one of our patients on retrospective review of MR images. Further study of MRI and sonographic correlation may highlight the presence of the sign with other MRI criteria of adenomyosis [11]. Fig. 6 46-year-old woman with menorrhagia., Coronal oblique sonohysterogram shows bright echogenic reflectors (arrow) that appeared within left myometrial wall during fluid injection. Finding suggests possibility of adenomyosis., xial T2-weighted fast spin-echo MR image (TR/TE, 2,800/85) shows two hyperintense foci (arrows) within thickened junctional zone on right side of uterus. lso evident is small fibroid (arrowhead) on left side. The most common sonographic finding in adenomyosis on SHG in our series was asymmetric myometrial thickening and heterogeneous echotexture (61%), as has been found in previous studies [10, 11]. The second most common findings were fluid-containing tracks or so-called myometrial cracks and myometrial cysts (26% each). The six patients (26%) in our series who had myometrial cracks on SHG had heavy uterine bleeding, which may be positively related to increasing depth of myometrial penetration. ll patients with this SHG finding had a junctional zone thickness greater than 12 mm and high-signal-intensity junctional zone cysts on T2-weighted MR images. Therefore, by distending the uterine cavity, separating parts of the anterior and posterior myometrium, and causing saline intravasation into these myometrial cracks, SHG facilitates understanding of the pathophysiologic mechanism of adenomyosis. Further prospective studies are needed to compare this sign with histopathologic findings. Other signs, such as an indistinct endometrial myometrial junction, were seen in only 22% of cases, fewer than in previous studies of TVS [3, 4], possibly because of more accurate differentiation of endometrium and myometrium on SHG. nother important observation was the bright echogenic foci that appeared within the myometrium during SHG of three of our patients (13%). These foci were not identified on MRI, which is performed without intrauterine contrast instillation. The presence of these echogenic foci suggested that adenomyosis might have been present because the foci were reminiscent of the deep diverticula and tracks of contrast material that can be seen on hysterosalpingography of patients with adenomyosis [12]. Correlation with MRI findings in our three cases showed that this finding does not always indicate the presence of adenomyosis at the site of the echogenic foci. Other causes of this finding are possible, including uplifting of the endometrium during catheterization of the uterine cavity, causing myometrial intravasation of air bubbles [13]. These hyperechoic foci appear rapidly and asymptomatically at the beginning of saline injection. Radiologists should be aware that this appearance is suggestive of but not specific for adenomyosis. If clinically indicated, MRI can be performed to assess for adenomyosis. In three of 26 women in our series, MRI showed small foci of adenomyosis when there were no signs of adenomyosis on SHG. We suggest this finding occurred because of the limited degree of involvement of the myometrium. SHG cannot be used to exclude the presence of early or focal adenomyosis. denomyosis is commonly associated with other gynecologic conditions, such as uterine fibroids and endometriosis [2]. Whether there is causation between these conditions or whether they simply represent common coexistent conditions is unclear. Confusion with fibroids is one of the most frequently encountered pitfalls in the diagnosis of adenomyosis [2]. In our series of patients, no women had large fibroids that obscured the findings of adenomyosis or interfered with evaluation of the extent of disease, although this problem has been reported in other studies comparing sonography and MRI in the evaluation of adenomyosis [8]. JR:192, pril 2009 1115
Verma et al. This study had limitations. First, cases of adenomyosis were identified by retrospective review of static images and reports from SHG and MRI studies. Therefore, the incidence of myometrial cracks may be greater than suggested in our study. Second, that histologic examination of the hysterectomy specimen is the ultimate reference standard may limit interpretation of our findings and may be a source of bias. However, we believe that by using MRI findings as the final arbiter for identification of adenomyosis, we minimized bias. Our results suggest that if MRI and expertise in interpretation of the images are available, the best available noninvasive option for preoperative assessment of adenomyosis is MRI. Moreover, follow-up MRI may be helpful for assessing the severity of adenomyosis and changes in signal intensity and junctional zone thickness and for avoiding misdiagnosis. MRI is an accurate noninvasive technique for monitoring response to treatment. ecause MRI is not always available and is not always appropriate as a first-line investigation of abnormal bleeding, maximizing recognition of adenomyosis at TVS and SHG is important. nother limitation of the study was that SHG findings were correlated with MRI and not with TVS findings. We took this approach because TVS was not performed on every patient. Future prospective analyses can address the relative accuracy, sensitivity, and specificity of TVS and SHG in the diagnosis of adenomyosis. That patients with abnormal bleeding or infertility commonly undergo evaluation with SHG represents an opportunity for recognizing the presence of adenomyosis. In our experience, when findings on SHG suggested adenomyosis, MRI findings confirmed the diagnosis in 96% cases. The appearance of focal bright reflectors, presumably air bubbles, in the myometrium during SHG in our small series correlated with the presence of focal adenomyosis on MRI in two of three cases, but the location of the reflectors did not match the location of focal adenomyosis on MR images. It is possible that air can enter the myometrium through patent endometrial gland channels not visible at MRI. This issue requires further study. previously unpublished, to our knowledge, SHG sign of adenomyosis is myometrial cracks. Knowledge of the appearances can enhance recognition of adenomyosis, decrease errors in interpretation, and improve management. This information is potentially useful because it can decrease the number of endometrial biopsies performed in cases in which SHG shows no endometrial abnormality and adenomyosis is the sole cause of abnormal bleeding. References 1. zziz R. denomyosis: current perspectives. Obstet Gynecol Clin North m 1989; 16:221 235 2. Vercellini P, Ragni G, Trespidi L, et al. denomyosis: a déjà vu? Obstet Gynecol Surv 1993; 48:789 794 3. azot M, Cortez, Emile D, et al. Ultrasonography compared with magnetic resonance imaging for the diagnosis of adenomyosis: correlation with histopathology. Hum Reprod 2001; 16:2427 2433 4. azot M, Dara E, Rouger J, Detchev R, Cortez, Uzan S. Limitations of transvaginal sonography for the diagnosis of adenomyosis, with histopathological correlation. Ultrasound Obstet Gynecol 2002; 20:605 611 5. Dueholm M, Lundorf E, Hansen ES, Ledertoug S, Olesen F. Evaluation of the uterine cavity with magnetic resonance imaging, transvaginal sonography, hysterosonographic examination, and diagnostic hysteroscopy. Fertil Steril 2001; 76:350 357 6. Dueholm M, Lundorf E, Sørensen JS, Ledertoug S, Olesen F, Laursen H. Reproducibility of evaluation of the uterus by transvaginal sonography, hysterosonographic examination, hysteroscopy and magnetic resonance imaging. Hum Reprod 2002; 17:195 200 7. Lev-Toaff S, Toaff ME, Liu J, Merton D, Goldberg. Value of sonohysterography in the diagnosis and management of abnormal uterine bleeding. Radiology 1996; 201:179 184 8. Chopra S, Lev-Toaff S, Ors F, ergin D. denomyosis: common and uncommon manifestations on sonography and magnetic resonance imaging. J Ultrasound Med 2006; 25:617 627 9. scher SM, rnold LL, Patt RH, et al. denomyosis: prospective comparison of MR imaging and transvaginal sonography. Radiology 1994; 190:803 806 10. Reinhold C, McCarthy S, ret PM, et al. Diffuse adenomyosis: comparison of endovaginal US and MR imaging with histopathologic correlation. Radiology 1996; 199:151 158 11 Reinhold C, Tafazoli F, Mehio, et al. Uterine adenomyosis: endovaginal US and MR imaging features with histopathologic correlation. Radio- Graphics 1999; 19[spec no]:s147 S160 12. Simpson WL Jr, eitia LG, Mester J. Hysterosalpingography: a reemerging study. RadioGraphics 2006; 26:419 431 13. Ors F, Lev-Toaff S, ergin D. Echogenic foci mimicking adenomyosis presumably due to air intravasation into the myometrium during sonohysterography. Diagn Interv Radiol 2007; 13:26 29 1116 JR:192, pril 2009