Uterine Smooth-Muscle Tumors with Unusual Growth Patterns: Imaging with Pathologic Correlation
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1 ohen et al. Imaging Pathologic orrelation of Uterine Tumors Women s Imaging Pictorial Essay 246.fm 12/1/06 WOMEN S IMGING Daniel T. ohen 1,2 Esther Oliva 3 Peter F. Hahn 1 rlan F. Fuller, Jr. 4 Susanna I. Lee 1 ohen DT, Oliva E, Hahn PF, Fuller F Jr, Lee SI Keywords: T, gynecologic imaging, leiomyoma, leiomyomatosis, MRI, oncologic imaging, sonography, uterine cancer, women s imaging DOI: /JR Received July 14, 2005; accepted after revision October 21, Department of Radiology, Massachusetts General Hospital, 55 Fruit St., White 270, oston, M Mallinckrodt Institute of Radiology, 510 S. Kingshighway lvd., Ninth Floor, St. Louis, MO ddress correspondence to D. T. ohen. 3 Department of Pathology, Massachusetts General Hospital, oston, M Gillette enter for Gynecologic Oncology, Gynecologic Oncology, Massachusetts General Hospital, oston, M JR 2007; 188: X/07/ merican Roentgen Ray Society Uterine Smooth-Muscle Tumors with Unusual Growth Patterns: Imaging with Pathologic orrelation OJETIVE. This essay illustrates the salient features of variant smooth-muscle tumors on multiple imaging techniques with correlative pathology. We describe how recognition of these features allows the radiologist to distinguish a uterine leiomyoma variant from the classic fibroid or a leiomyosarcoma. Finally, we highlight the role of the radiologist in triaging these patients to surgical versus medical management and in surgical planning. ONLUSION. Parasitic leiomyoma, intravenous leiomyomatosis, disseminated peritoneal leiomyomatosis, and benign metastasizing leiomyoma show key features on multiple imaging techniques that correlate with pathology findings. In the appropriate clinical setting, the radiologist should include these unusual lesions in the broader differential diagnosis of smoothmuscle tumors and, in certain cases, aid in surgical planning. he spectrum of smooth-muscle tumors arising from the uterus ranges T from benign leiomyoma to malignant leiomyosarcoma but also includes a variety of lesions with growth patterns that extend outside the uterus, including parasitic leiomyoma, intravenous leiomyomatosis, disseminated peritoneal leiomyomatosis, and benign metastasizing leiomyoma. These benign tumors resemble typical uterine leiomyomas at both gross and microscopic levels. However, the atypical location and aggressive growth of these variant tumors present a diagnostic dilemma and have led to controversy regarding their pathogenesis and actual benignity. ecause these benign smooth-muscle tumors are rare, no series describing their imaging characteristics has been reported, to our knowledge. This essay illustrates the salient features of these tumors on multiple imaging techniques with correlative pathology. We describe how recognition of these features allows the radiologist to distinguish a uterine leiomyoma variant from the classic fibroid or a leiomyosarcoma. Finally, we highlight the role of the radiologist in triaging these patients to surgical versus medical management and in surgical planning. Parasitic Leiomyoma Parasitic leiomyomas present as peritoneal pelvic benign smooth-muscle masses separate from the uterus. parasitic leiomyoma likely originates as a pedunculated subserosal leiomyoma that twists and torses from its uterine pedicle. Now, free in the peritoneal cavity, it survives by recruiting neovascularization from adjacent structures. The originating pedunculated fibroid likely develops premenopausally, whereas the parasitic leiomyoma may become clinically evident either before or after menopause. On imaging, parasitic leiomyoma shows tissue characteristics similar to uterine leiomyoma. ecause of their multiplanar capabilities, T and MRI can show the location of the tumor relative to adjacent structures, which may be critical for surgical planning (Fig. 1). The differential diagnosis of parasitic leiomyoma varies with its location but can include ovarian stromal tumor, leiomyosarcoma, drop metastases, and lymphadenopathy. With behavior similar to uterine leiomyoma, parasitic leiomyoma may recur after resection or, conversely, may show hormoneresponsive behavior, including size stability or even shrinkage with natural, surgical, or chemical menopause [1] (Fig. 2). Surgery is usually performed for symptomatic relief or to prevent impingement of vital structures. Intravenous Leiomyomatosis Intravenous leiomyomatosis is defined by a proliferation of benign smooth muscle within veins outside the confines of a leiomyoma or even when no leiomyoma is present. Intrave- 246 JR:188, January 2007
2 Imaging Pathologic orrelation of Uterine Tumors Fig. 1 Parasitic leiomyoma in 52-year-old woman with distant history of hysterectomy who presented with pelvic masses., Transverse transabdominal sonographic image of pelvis shows 5-cm right pelvic parasitic leiomyoma (arrows) indenting bladder (star). Heterogeneous echotexture of parasitic leiomyoma is similar to that of uterine fibroid., Sagittal fast spin-echo T2 MR image shows left pelvic parasitic leiomyoma (solid arrow) deforming bladder. Mass shows intermediate signal intensity that is slightly brighter than that of muscle. Internal swirling pattern is common for leiomyoma and is atypical for ovarian fibroma, which is usually homogeneously hypointense on T1 and T2 and without swirl pattern on contrast-enhanced or T2 images. Posterior aspect of mass abuts vagina (open arrow). Note close proximity of tumor to bladder wall (arrowheads). With this information, urologist was consulted preoperatively to repair cystostomy necessitated by tumor resection., xial gradient-echo MR image obtained with fat saturation and gadolinium enhancement shows homogeneous hyperintense enhancement (star) after dynamic gadolinium injection that is similar to intrauterine fibroid. Rectum (arrow) is seen posteriorly. Fig. 2 Parasitic leiomyoma in 39-year-old woman with history of myomectomy who presented with pelvic masses. oronal gradient-echo fat-suppressed gadolinium-enhanced T1-weighted MR image reveals multiple parasitic leiomyoma tumors. Note right adnexal tumor (asterisk), right pararectal tumor (star), and bilateral ischiorectal fossa tumors (arrowheads) in relation to uterine fundus (arrow). Tumors were stable on imaging over 9 months and clinically for years on medical management. nous leiomyomatosis may even extend outside the uterus (Fig. 3). Intravenous leiomyomatosis may show significant involvement of peritoneal structures, but it is most dramatic when there is intracardiac extension via the inferior vena cava [2]. The implications for increased risk of deep vein thrombosis are unknown because of low case numbers, although we have observed deep venous thromboses in these patients. If intravenous leiomyomatosis arises and remains solely in the uterus, a radiologic diagnosis is difficult because the tumor mimics a typical leiomyoma. If intrauterine intravenous leiomyomatosis is incidentally diagnosed on pathologic examination from a routine hysterectomy, one could consider interval surveillance examinations to assess for recurrence. However, given the benign indolent course of this disease, it is reasonable to defer imaging until there is a symptomatic indication. JR:188, January
3 ohen et al. Sonography may be sufficient for detecting atypical features of intravenous leiomyomatosis, such as extrauterine extension. The initial route outside the uterus for intrauterine intravenous leiomyomatosis may include the broad ligament veins (Fig. 4). The broader field of view of MRI and T compared with sonography details additional anatomic relationships that are required for surgical planning. s with parasitic leiomyoma, intravenous leiomyomatosis may recur after resection and may also show hormone responsiveness. The salient macroscopic feature that distinguishes parasitic leiomyoma and extrauterine intravenous leiomyomatosis is detectable evidence of extension into a vein. The prognostic significance of differentiating between these lesions is not known given the few reported cases. Fig. 3 Intravenous leiomyomatosis in 43-year-old woman with history of hysterectomy at which intravenous leiomyomatosis was diagnosed histologically in uterus and who presented 1 year later with retroperitoneal mass., xial fast spin-echo T2-weighted MR image shows bulky retroperitoneal tumor with solid and fluid components; arrows delineate tumor edge. T2 hyperintense components illustrate cystic areas (asterisks)., Obtained craniad to, axial gradient-echo fat-suppressed T1-weighted image with dynamic gadolinium enhancement shows hypervascular tumor enhancement of solid components (black asterisk) and nonenhancement of cystic components (white asterisks) in this retroperitoneal intravenous leiomyomatosis tumor; solid arrows delineate tumor edge. Intravenous leiomyomatosis abuts and deforms slitlike T1 hyperintense inferior vena cava (arrowhead) adjacent to distal aorta (open arrow). lthough intravascular component of tumor is not seen on imaging, excision required inferior vena cava venotomy and creation of neoileal ureter for resection., Gross macroscopic image of firm, white intravenous leiomyomatosis shows swirling smooth muscle components and multifocal cystification; arrows denote cyst edge. This cyst is seen as T2 hyperintensity () and T1 hypointensity () on preoperative MRI. Metal stent (arrowhead) passes through ureter seen on opposite side of mass. 248 JR:188, January 2007
4 Imaging Pathologic orrelation of Uterine Tumors Disseminated Peritoneal Leiomyomatosis Discrete nodules of benign smooth muscle scattered over the peritoneum characterize classic disseminated peritoneal leiomyomatosis. However, disseminated peritoneal leiomyomatosis presents a protean appearance, sometimes presenting as tiny peritoneal nodules mimicking peritoneal carcinomatosis or as bulky intra- or extraperitoneal masses resembling leiomyosarcoma [3, 4] (Figs. 5 and 6). Disseminated peritoneal leiomyomatosis is classically seen in premenopausal patients and is frequently seen in pregnant women. Disseminated peritoneal leiomyomatosis likely is the result of Fig. 4 Intravenous leiomyomatosis in 47-year-old woman with intrauterine intravenous leiomyomatosis previously diagnosed histologically and who presented with palpable pelvic mass and abnormal vaginal bleeding., oronal transvaginal sonographic image with color Doppler imaging shows increased vascularity (arrows) within mass. and, xial fast spin-echo T2-weighted () and axial gradient-echo T1-weighted with fat saturation and gadolinium enhancement () MR images show heterogeneous leiomyomatous uterus (leiomyoma edge, open arrows, ; endometrial canal, arrowhead, ). Our standard pelvic MR protocol includes up to 10 ml (0.1 mmol/kg) of IV gadolinium chelate with power injection at 4 ml/s and dynamic imaging at 20, 70, and 180 seconds. Intravenous leiomyomatosis (solid arrows, ) and other smooth-muscle tumors enhance similarly to nonnecrotic leiomyoma or myometrium (asterisk, ). Extrauterine extension of intravenous leiomyomatosis into broad ligament (solid arrows, ) resulted in triage of patient to open laparotomy over vaginal or laparoscopic resection. (Fig. 4 continues on next page) multifocal metaplasia of the peritoneum. However, some authors promote a disseminated origin from a single lesion [4]. The tiny peritoneal nodules of disseminated peritoneal leiomyomatosis may be below the resolution of all radiologic techniques. Incidental discovery during surgery is not rare [3, 4]. When the disseminated JR:188, January
5 ohen et al. D Fig. 4 (continued) Intravenous leiomyomatosis in 47-year-old woman with intrauterine intravenous leiomyomatosis previously diagnosed histologically who presented with palpable pelvic mass and abnormal vaginal bleeding. D, Gross macroscopic image shows white tan lobulated mass (stars) fills and distends right broad ligament vein; thin red wall of vein is denoted by arrowheads. E, H and E histologic image shows parauterine broad ligament vein lined by endothelium (arrowheads) is distended by benign smooth-muscle proliferation (asterisk) of intravenous leiomyomatosis. Fig. 5 Disseminated peritoneal leiomyomatosis in 36-year-old woman who presented with abdominal pain and intraperitoneal soft-tissue nodules., IV contrast enhanced axial T image shows round, solid, enhancing mass (arrowheads) adjacent to sigmoid colon (arrow)., xial image from 18 F-FDG PET/T examination shows 6- and 12-mm disseminated peritoneal leiomyomatosis nodules (arrows) without increased metabolic 18 F-FDG uptake. Increased 18 F-FDG uptake (red) is seen on this fusion image; for example, loop of small bowel shows physiologic intestinal uptake (arrowhead). Lack of 18 F-FDG avidity makes malignancy, such as leiomyosarcoma, less likely. However, malignancy can be definitively excluded only with histologic sampling. (Fig. 5 continues on next page) E 250 JR:188, January 2007
6 Imaging Pathologic orrelation of Uterine Tumors peritoneal leiomyomatosis nodules are of sufficient size, approximately 6 mm or larger, 18 F-FDG PET/T may be used to distinguish isometabolic activity of disseminated peritoneal leiomyomatosis from hypermetabolic uptake of leiomyosarcoma [5] (Fig. 5). Disseminated peritoneal leiomyomatosis nodules can be distinguished from endometriosis because they do not show the marked T1 hyperintensity that is seen with the latter entity. Nevertheless, direct sampling is required for definitive diagnosis and to exclude malignancy. Hormonal blockade is often an effective treatment with or without surgical debulking. Fig. 5 (continued) Disseminated peritoneal leiomyomatosis in 36-year-old woman who presented with abdominal pain and intraperitoneal soft-tissue nodules., Intraoperative photograph obtained during laparotomy shows round mass (arrowheads), as seen on T (), and 4-mm radiologically occult small nodules on peritoneal lining (arrows). D, Gross macroscopic image shows smooth-muscle character (asterisks) of firm white intraperitoneal mass, which abuts sigmoid colon, with its wall (arrowheads) and lumen (arrow) noted. enign Metastasizing Leiomyoma enign metastasizing leiomyoma classically has been described as incidental pulmonary nodules in women with a history of uterine leiomyomas [6]. Pathologically, these nodules are composed of benign smooth muscle similar to leiomyoma. enign metastasizing leiomyoma can have a benign indolent clinical course with longterm stability. s with disseminated peritoneal leiomyomatosis, there is controversy in the medical literature regarding the pathogenesis of benign metastasizing leiomyoma. Does it represent multifocal metaplasia or, as the name suggests, is it a metastatic phenomenon secondary to vascular invasion within a uterine leiomyoma [7]? Radiographically, benign metastasizing leiomyoma presents typically as solitary or multiple pulmonary nodules, and on T these nodules enhance homogeneously (Fig. 7). enign metastasizing leiomyoma can be seen as soft-tissue implants in the pleura (Fig. 8) and on solid abdominal viscera (Fig. 9). lthough the multiplicity of lesions raises the question of metastatic disease, in the clinical setting of a hormonally active woman with a history of uterine leiomyomas and no known primary malignancy, the radiologist can add benign metastasizing leiomyoma to the diagnostic considerations even before tissue sampling. enign metastasizing leiomyoma can be seen in patients with intravenous leiomyomatosis. In one patient in our series, imaging showed uterine intravenous leiomyomatosis and foci of pulmonary benign metastasizing leiomyoma (Fig. 9). Whether there is progression from wholly intrauterine to extrauterine intravenous leiomyomatosis with macroscopic venous extension to disseminated disease (e.g., benign metastasizing leiomyoma) is unknown. lthough it is intellectually appealing to propose such a continuum, there is controversy in the pathology literature regarding this point. onclusion Parasitic leiomyoma, intravenous leiomyomatosis, disseminated peritoneal leiomyomatosis, and benign metastasizing leiomyoma are rare histologically benign smooth-muscle tumors. Their variant nature stems from their location and unusual growth patterns either outside the uterus or within veins. They typically show indolent growth that is often hormonally responsive; frequently develop in premenopausal women; and often regress with medical hormonal blockade, oophorectomy, or natural menopause. On imaging, these tumors mimic uterine fibroids, with well-defined margins and hypervascular smooth-muscle characteristics. However, the growth patterns of these leiomyoma variants can imitate those of more aggressive cancers: Disseminated peritoneal leiomyomatosis can resemble peritoneal carcinomatosis, parasitic leiomyoma or intravenous leiomyomatosis can D JR:188, January
7 ohen et al. Fig. 6 Disseminated peritoneal leiomyomatosis in 48-year-old woman with history of myomectomy who presented 1 year later with intra- and retroperitoneal soft-tissue masses., Transverse transvaginal sonographic image of pelvis shows heterogeneous leiomyomatous uterus (arrows) and left hydrosalpinx (star) caused by left pelvic and retroperitoneal mass (not shown). and, IV and oral contrast-enhanced axial T image () and coronal reformation image () show left retroperitoneal mass (solid arrows). Tumor shows intense enhancement typical of leiomyoma. entral low attenuation (asterisk, ) may indicate central degeneration or ischemia. Tumor encases and displaces dilated left gonadal vein (open arrow) laterally from aorta (arrowhead). D, oronal fast spin-echo T2-weighted MR image reveals that both left pelvic and retroperitoneal masses (open and solid arrows, respectively) show intermediate gray signal intensity that is slightly brighter than that of muscle. Uterine myometrium shows multiple small T2 hypointense intramural leiomyomas (solid arrowhead) and mild distortion of endometrial stripe (open arrowhead). (Fig. 6 continues on next page) D 252 JR:188, January 2007
8 Imaging Pathologic orrelation of Uterine Tumors E Fig. 6 (continued) Disseminated peritoneal leiomyomatosis in 48-year-old woman with history of myomectomy who presented 1 year later with intra- and retroperitoneal soft-tissue masses. E, Gross macroscopic image shows that two well-defined medium-sized 10- and 8-mm nodules (arrows) that were not detected on imaging are present in mesentery (asterisk) of bowel. Note smooth-bowel wall serosa (arrowhead). F, H and E histologic image shows fascicles of benign smooth muscle forming mass (asterisk) in lymph node. Note residual lymph node (arrow) with blue lymphocytes. Fig. 7 enign metastasizing leiomyoma in 54-year-old woman who underwent hysterectomy 14 years earlier and was found to have incidental pulmonary nodules that had been stable for more than 10 years. Several nodules were resected soon after their initial incidental discovery for histologic diagnosis., Frontal radiograph with digital magnification view shows multiple 14- and 8-mm pulmonary nodules (arrowheads) of benign metastasizing leiomyoma., IV contrast enhanced axial T image in lung windows shows numerous randomly distributed, smooth, rounded nodules (arrows) that are characteristic of benign metastasizing leiomyoma. (Fig. 7 continues on next page) F JR:188, January
9 ohen et al. resemble leiomyosarcoma, intravenous leiomyomatosis can resemble renal cell carcinoma in the setting of inferior vena cava involvement, and benign metastasizing leiomyoma can resemble pulmonary or hepatic metastatic disease. Thus, diagnosis requires a radiologist to be aware of these entities and to include them in the differential diagnosis in the appropriate clinical setting. Fig. 7 (continued) enign metastasizing leiomyoma in 54-year-old woman who underwent hysterectomy 14 years earlier and was found to have incidental pulmonary nodules that had been stable for more than 10 years. Several nodules were resected soon after their initial incidental discovery for histologic diagnosis., Gross macroscopic image shows that whitish-gray well-defined mass (arrows) is present in lung parenchyma (asterisks). D, H and E histologic image shows bland smooth-muscle cells are arranged in fascicles (arrows) and entrap alveolar epithelium (arrowheads) at periphery. ecause the imaging findings of parasitic leiomyoma, intravenous leiomyomatosis, disseminated peritoneal leiomyomatosis, and benign metastasizing leiomyoma overlap with those of malignancy, these entities require direct pathologic sampling for diagnosis. Once a diagnosis is histologically confirmed, patients can be triaged to medical hormonal management or can undergo Fig. 8 enign metastasizing leiomyoma in 48-year-old woman who was found to have pleural masses with benign smooth-muscle histology on biopsy. Left hemithorax pleural masses (arrows) seen on IV contrast-enhanced axial T image were classified as benign metastasizing leiomyoma after hysterectomy, which revealed multiple intramural leiomyomas. surgical excision based on lesion location, degree of involvement of surrounding structures, and the severity of the patient s comorbid conditions. Multiplanar imaging depicts key anatomic points, such as ureter, bladder, or vessel involvement, that are crucial for surgical planning. When presented with the radiologic appearance of locally aggressive or metastatic tu- D 254 JR:188, January 2007
10 Imaging Pathologic orrelation of Uterine Tumors mors with smooth-muscle characteristics in a woman with a history of fibroids, the radiologist should broaden the differential diagnosis to include variant uterine smooth-muscle tumors. References 1. Wilkinson N, Rollason TP. Recent advances in the pathology of smooth muscle tumors of the uterus. Histopathology 2001; 39: Lam P, Lo K, Yu M, et al. IV leiomyomatosis: two cases with different routes of tumor extension. J Fig. 9 enign metastasizing leiomyoma in 34-year-old woman with pathologically proven pulmonary benign metastasizing leiomyoma nodules found to have liver and adrenal nodules that remained slowly growing on imaging over 5-year period. and, xial arterial phase IV contrast-enhanced T () and T1-weighted gadolinium-enhanced MR () images show hypervascular enhancing 1.5-cm mass in segment VI of right lobe of liver (circle) and 2.5-cm enhancing right adrenal mass (solid arrow). Note appearance of inferior vena cava (open arrow) and aorta (asterisk) during arterial phase. Vasc Surg 2004; 39: Fuller Jr., Patterson D, Shimm D. Sarcomas of the female genital tract. In: Raaf J, ed. Soft tissue sarcomas: diagnosis and treatment. St. Louis, MO: Mosby, 1993: ltinok G, Usubutun, Kucukali T, et al. Disseminated peritoneal leiomyomatosis: a benign entity mimicking carcinomatosis. rch Gynecol Obstet 2000; 264: Naohiko U, Tetsuji T, Masato M. Positron emission tomography with 18 F-FDG of uterine sarcoma: a comparison with magnetic resonance imaging and power Doppler imaging. Gynecol Oncol 2001; 80: bramson S, Gilkeson R, Goldstein JD, Woodard PK, Eisenberg R, bramson N. enign metastasizing leiomyoma: clinical, imaging, and pathologic correlation. JR 2001; 176: anzonieri V, D more ES, artoloni G, Piazza M, landamura S, arbone. Leiomyomatosis with vascular invasion: a unified pathogenesis regarding leiomyoma with vascular microinvasion, benign metastasizing leiomyoma and intravenous leiomyomatosis. Virchos rch 1994; 425: JR:188, January
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