Patterns of Soft-Tissue Tumor Extension in and out of the Pelvis

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1 Musculoskeletal Imaging Pictorial Essay Sugawara et al. Imaging of Soft-Tissue Tumor Extension Musculoskeletal Imaging Pictorial Essay Shunsuke Sugawara 1,2 Shigeru Ehara 1 Shin Hitachi 1 Kyoji Okada 3 Sugawara S, Ehara S, Hitachi S, Okada K Keywords: CT, MRI, pelvis, soft-tissue tumor DOI: /AJR Received February 15, 2009; accepted after revision August 17, Department of Radiology, Iwate Medical University School of Medicine, 19-1 Uchimaru, Morioka, Iwate , Japan. Address correspondence to S. Ehara (ehara@iwate-med.ac.jp). 2 Present address: Department of Radiology, Ebara Hospital, Tokyo, Japan. 3 Department of Orthopedic Surgery, Akita University School of Medicine, Akita, Japan. AJR 2010; 194: X/10/ American Roentgen Ray Society Patterns of Soft-Tissue Tumor Extension in and out of the Pelvis OBJECTIVE. The purpose of this article is to present the route of extension in nine softtissue tumors and tumorlike lesions of the pelvic wall. CONCLUSION. Soft-tissue tumors of the pelvis, particularly malignant ones, extend into other compartments through specific pathways that are bordered by bones, ligaments, and fasciae. Such pathways include the greater sciatic foramen, the obturator foramen, the femoral canal, the muscular lacuna, the pelvic outlet, and the inguinal canal. T umors in the pelvis consist of tumors arising from pelvic organs (such as male and female reproductive organs, urinary bladder, and rectum) and soft-tissue tumors of the pelvic wall. Intraperitoneal and retroperitoneal tumors of the upper abdomen may also extend into the pelvis. In particular, soft-tissue tumors may involve both the inside and outside of the pelvis, and such transcompartmental spread is an important factor for treatment planning. The objectives of this article are to present the patterns of soft-tissue tumor extension and to assess the possibility of differential diagnosis by such an extension pattern [1]. Materials and Methods Because no intervention or effect on the treatment of patients was involved in this retrospective analysis, institutional review board approval and consent from the patients were not required at the time of this study. Legislation on personal data protection was followed. Soft-tissue (mesenchymal and peripheral nerve) tumors and tumorlike conditions involving the pelvic cavity, pelvic wall, and extrapelvic space on CT, MRI, or both were included in this study. Adequate CT or MRI studies to reveal the extent of the lesions and histologic diagnoses were available in all the cases. Lesions involving the intraperitoneal cavity or retroperitoneum extending into the pelvis were excluded. Such cases were identified in our teaching collections and by a computer search of radiology reports. Because these images were obtained at five different institutions, scanning techniques were not standardized. Imaging findings were evaluated by three radiologists (one skeletal radiologist with more than 20 years of experience, one junior faculty member with 2 years of experience in skeletal radiology, and one resident). Any differences in interpretation were settled by consensus. The imaging findings were analyzed to assess tumor extent, and the route of tumor extension was categorized according to the seven possibilities discussed in the Anatomy section of this article. Correlation with surgical findings, which were available only in the resected cases, was not performed. Because of the limitations in the methodology of data collection, statistical analysis was not performed. Anatomy In this article, the pelvic cavity is the true pelvis, which is defined as follows: the inlet of the pelvis bordered by terminal line of the pelvis (Fig. 1) and outlet of the pelvis bordered by the anterior pubic arch, the ischial tuberosities, and the coccyx [2]. The bony pelvis is composed of the innominate (coxal) bones and the sacrum [3]. The true pelvic cavity is below the terminal line of the pelvis that represents the caudal border of the iliac fossa. The terminal line of the pelvis is bounded by the promontory, iliopubic eminence, pecten pubis, and superior border of the pubic symphysis. Pelvic tumors, especially malignant ones, mainly extend into the adjacent compartment through the anatomically weak regions, including the hiatus composed of bone, ligament, muscle, and fascia. Normally, blood vessels, nerves, lymphatic vessels, and muscles pass the hiatus, but this may also be a route by which tumors spread. 746 AJR:194, March 2010

2 Imaging of Soft-Tissue Tumor Extension Greater Sciatic Foramen The greater sciatic foramen (Fig. 2) is bordered by the greater sciatic notch, sacrospinous ligament (sacrum ischial spine), and sacrotuberous ligament (sacrum ischial tuberosity). This foramen is divided into the superior and inferior piriform foramina by the piriform muscle and the superior and inferior gluteal artery, vein, and nerve; the internal pudendal artery or vein; and the sciatic nerve, all of which pass through the foramen. The greater sciatic foramen is a route of tumor extension between the pelvic cavity and the gluteal region [1] (Fig. 3). The lesser sciatic foramen is bordered by the lesser sciatic notch, the sacrospinous ligament, and the sacrotuberous ligament. It is a route of tumor extension between the gluteal region and the perineum and does not extend into the pelvis. Obturator Foramen The obturator foramen (Fig. 4) is closed by the obturator membrane, except for the obturator canal, through which the obturator artery, vein, and nerve pass. Outer and inner aspects of the obturator foramen are covered by the external and internal obturator muscles. The obturator canal, or foramen, is a route of tumor extension between the pelvic cavity and the medial aspect of the thigh [1, 4] (Fig. 5). Femoral Canal The femoral canal (Fig. 6) is a route connecting the pelvic cavity and the anteromedial aspect of the thigh (Fig. 7). It consists of the muscular lacuna (containing the iliopsoas muscle and the femoral nerve) and the vascular lacuna (containing the femoral artery and vein and lymphatic vessels) and is bounded by the inguinal ligament, anterior edge of the innominate bones, and iliopectineal arch dividing it into two lacunae. The medial vascular lacuna contains the femoral duct and occupied by loose connective and adipose tissues. Lymphatic vessels pass through the femoral canal. The muscular lacuna is bounded by the inguinal ligament, anterior edge of the innominate bones, and the iliopectineal arch. The iliopsoas muscle and the femoral nerve pass through this lacuna. The iliopsoas muscle is covered by the iliac fascia, and soft-tissue tumors arising in the iliopsoas muscle extend into the anterior aspect of the thigh through this lacuna (Fig. 8). Pelvic Outlet The pelvic outlet (Fig. 9) is covered by the pelvic diaphragm, urogenital diaphragm, and visceral and parietal fascia. The pelvic diaphragm consists of the levator ani and coccygeal muscles and their fascia. Because of disuse of the coccygeal muscle, a small gap exists between the levator ani muscle and the coccygeal muscle and is covered only by the fascia. An abscess in the ischioanal fossa extends into the pelvis [5]. Similarly, a neoplasm in the pelvis also potentially extends into the perineum through this gap by invading the muscles. The pelvic outlet is a route of tumor extension between the pelvic cavity and the perineum [5, 6] (Fig. 10). Inguinal Canal The inguinal canal (Fig. 11) consists of abdominal wall muscle, fascia, and inguinal ligament. It contains the spermatic cord or the round ligament of the uterus. The pelvic cavity leads to the perineum (scrotum or large pudendal lip) through the inguinal canal. Soft-tissue tumors in the pelvic cavity may also extend into the perineum through the inguinal canal [1, 7] (Fig. 12). Extension Along Nerves and Blood Vessels Tumors arising from the nerve can extend to any other compartments along the nerve [8]. Because nerves pass though the hiatus, perineural extension is also seen in the spinal canal (Fig. 13). Tumors arising from blood vessels (e.g., leiomyosarcoma) may also extend to other compartments along the blood vessels [9]. Extension Through the Weak Bone (Transosseous Extension) Infiltrating tumors may extend in or out of the pelvis through the thin portion of the bony pelvis, particularly the thin iliac wing. Such tumors are most often malignant mesenchymal tumors in the pelvic wall and extend into adjacent compartments directly (Fig. 14). Results Our series of nine cases included three men and one boy and five women (age range, years; median age, 48 years). Histology of the lesion and the pattern of tumor extension are summarized in Table 1. Three cases were benign, and the rest were malignant. Three cases extended into the adjacent compartment through two or more pathways. Tumor extension through the greater sciatic foramen was seen in three cases; obturator foramen in three; pelvic outlet in one; and femoral canal, muscular lacuna, and inguinal canal in one each. Transosseous extension was seen in two cases. In the case of neurofibroma, the tumor extended along nerves. Malignant tumors revealed transcompartmental spread more frequently. Transosseous extension of a benign lesion was extremely uncommon and may be seen in unusual cases such as patient 6. Although the obturator foramen was a route of hernia of pelvic organs, only malignant tumors extended through it. Specific imaging diagnoses were possible in two lipomatous tumors and neurofibromatosis on the basis of the imaging findings. Discussion Soft-tissue tumors extending in and out of the pelvis were mainly malignant tumors. The hiatus of the pelvis was the main route of transcompartmental spread. These routes were similar to the pathways through which inflammation spread to other compartments [10]. Bones, ligaments, and fasciae were the natural barrier of tumor invasion, but muscles were often invaded by TABLE 1: Histology and Pattern of Tumor Extension in Nine Patients Patient No. Age (y) Sex Disease Route 1 10 M Myositis ossificans Muscular lacuna 2 18 M Neurofibromatosis Greater sciatic foramen (along sciatic nerve) 3 22 F Well-differentiated liposarcoma Obturator foramen 4 36 M Malignant peripheral nerve sheath tumor Femoral duct, pelvic outlet, obturator foramen, transosseous (pubis) 5 48 F Fibrosarcoma (recurrence) Greater sciatic foramen 6 53 F Hibernoma Greater sciatic foramen, transosseous (ilium) 7 66 F Malignant fibrous histiocytoma (pleomorphic undifferentiated sarcoma) Greater sciatic foramen 8 70 F Synovial sarcoma Obturator foramen 9 71 M Liposarcoma Inguinal canal AJR:194, March

3 Sugawara et al. infiltrating tumors. In our series, the piriform muscle and the levator ani muscle were hard to identify because of tumor invasion. The extent and size of the tumor were important for planning for surgical excision and radiation therapy. For the staging of mesenchymal tumors of the pelvic wall, there were two systems used. In the Musculoskeletal Tumor Society system described by Enneking et al. [11], extracompartmental spread of a T2 lesion was assigned a higher stage. This system was better suited for soft-tissue tumors in the extremities than those in the trunk. In the American Joint Committee on Cancer system described by Greene et al. [12], the localization (deep vs superficial) and the size (> 5 cm or 5 cm) were used to assess the T factor (the primary lesion). All the malignant cases in this series were T2b lesions, deep tumors larger than 5 cm. As seen in our series, tumors with extracompartmental spread were often malignant, and the extensive mesenchymal tumors were not amenable to eradication with an adequate resection margin. However, there may be a higher chance of control with the advancement of chemotherapy and radiation therapy. Because the case numbers were small in our series, it was difficult to characterize histologic features related to the pattern of tumor extension. Tumors extending by bone destruction are usually malignant, and the bone destruction may be massive. Transosseous extension of benign tumors is extremely uncommon, including penetration of the thin ilium and the dilatation of nerve foramina in the case of hibernoma. Except for such an unusual case, transosseous spread is a sign of malignancy. In addition, in our series, tumor extension through the obturator foramen was present only in the malignant tumor. Extension of benign soft-tissue tumors through the obturator foramen was not observed in any case. But a previous report showed the hibernoma of the thigh extended into the pelvis through the obturator foramen [4]. In all of our cases, the margin between the tumors and fasciae or the serous membrane were well defined, even in malignant tumors, and fasciae and serous membrane were effective barriers of tumor invasion. Hence, it is thought that the obturator membrane is resistant to tumor invasion, and tumors with high malignant potential are expected to extend through the obturator foramen. Because the obturator canal is not an anatomically weak structure, benign soft-tissue tumor may not extend easily into other compartments through the obturator canal (or foramen). Theoretically, tumor extension along the vessels and nerves may be observed in all the routes in which nerves or vessels exist. Previous reports showed that some soft-tissue tumors such as leiomyosarcoma extended into the vessel lumen [9]. In addition, neurofibroma extended through the neural foramina of the sacrum. The obturator nerve and vessel run through the obturator canal, and we think that a tumor extending through the obturator canal tends to extend along the vessels and nerves. However, that is still not certain. Limitations of this study include the small number of cases, lack of pathologic correlation, and lack of correlation with tumor staging. In addition, the case series in this report are based on the teaching collections of different institutions consisting of relatively rare cases, and they do not necessarily reflect a representative case series of this tumor category. Conclusions Soft-tissue tumors, often malignant, extend in and out of the pelvis through the greater sciatic foramen, obturator foramen, femoral canal, muscular lacuna, pelvic outlet, and inguinal canal. In addition, infiltrating tumors extend into the adjacent compartments by the destruction of small or thin bones, including the ilium and the pubis. Transosseous extension and extension through the obturator foramen are more frequently malignant. Extension through blood vessels and nerves is seen in specific tumors. Acknowledgments We thank Kunihiko Fukuda of Tokyo, Japan; Susan Kattapuram of Boston, MA; and William Reinus of Philadelphia, PA, for allowing us to use their cases. References 1. Lewis SJ, Wunder JS, Couture J, et al. Soft tissue sarcomas involving the pelvis. J Surg Oncol 2001; 77: Standing S, ed. Gray s anatomy: the anatomical basis of clinical practice, 39th ed. Edinburgh, Scotland: Elsevier, 2005: Pozniak M, Petasnick JP, Matalon TAS, Bayard WJ. Computed tomography in the differential diagnosis of pelvic and extrapelvic disease. Radio- Graphics 1985; 5: Mugel T, Ghossain MA, Guinet C, et al. MR and CT findings in a case of hibernoma of the thigh extending into the pelvis. Eur Radiol 1998; 8: Lluager J, Palmer J, Pérez C, Monill JM, Ribé J, Moreno A. The normal and pathologic ischiorectal fossa at CT and MRI imaging. RadioGraphics 1998; 18: Outwater EK, Marchetto BE, Wagner BJ, Siegelman ES. Aggressive angiomyxoma: findings on CT and MRI imaging. AJR 1999; 172: Hassan JM, Quisling SV, Melvin WV, Sharp KW. Liposarcoma of the spermatic cord masquerading as an incarcerated inguinal hernia. Am Surg 2003; 69: Emory TS, Scheithauer BW, Hirose T, Wood M, Onofrio BM, Jenkins RB. Intraneural perineurioma: a clonal neoplasm associated with abnormalities of chromosome 22. Am J Clin Pathol 1995; 103: McDonald DK, Kalva SP, Fan CM, Vasilyev A. Leiomyosarcoma of the uterus with intravascular tumor extension and pulmonary tumor embolism. Cardiovasc Intervent Radiol 2007; 30: Rotstein OD, Pruett TL, Simmons RL. Thigh abscess: an uncommon presentation of intraabdominal sepsis. Am J Surg 1986; 151: Enneking WF, Spanier SS, Goodman MA. A system for the surgical staging of musculoskeletal sarcoma. Clin Orthop Relat Res 1980; 153: Greene FL, Page DL, Fleming FD, et al. American Joint Committee on Cancer: cancer staging manual, 6th ed. New York, NY: Springer-Verlag, 2002: AJR:194, March 2010

4 Imaging of Soft-Tissue Tumor Extension Fig. 1 Drawing shows anatomy of pelvis, composed of pair of innominate bones and sacrum. True pelvis (circle) is below terminal line of pelvis. Fig year-old woman with malignant fibrous histiocytoma. There is tumor extension through greater sciatic foramen. Axial contrast-enhanced CT image shows tumor (asterisk) in gluteal region extending into pelvis through greater sciatic foramen (arrow). Tumor transgresses sciatic notch above ischial spine (above sacrospinous ligament). Piriform muscle cannot be identified because of tumor invasion. Bone destruction is not noted. Fig. 2 Drawing shows greater sciatic foramen is bounded by greater sciatic notch, sacrospinous ligament (dotted line), and sacrotuberous ligament (dashed line). Greater sciatic foramen is route of tumor extension (arrows) between pelvis and gluteal region. Fig. 4 Drawing shows obturator foramen is closed by obturator membrane. Obturator artery, vein, and nerve pass through obturator canal, which is hiatus of obturator membrane. Obturator foramen is route of tumor extension (arrows) between pelvis and medial aspect of thigh. AJR:194, March

5 Sugawara et al. Fig. 5 Synovial sarcoma extending through obturator foramen in 70-year-old woman. Coronal T1-weighted MR image after IV gadolinium administration shows tumor (asterisk) extending through obturator foramen (arrow). A Fig. 6 Drawing shows femoral canal and muscular lacuna. Vascular lacuna (medial fine dot) and muscular lacuna (lateral rough dot) are bounded by inguinal ligament (inguinal canal) and anterior edge of innominate bones. These two laminae are divided by iliopectineal arch. Medial vascular lacuna, containing femoral duct (dashed circle), may be route of tumor extension between pelvis and anteromedial aspect of thigh. Muscular lacuna may be route of tumor extension between pelvis and anterior aspect of thigh. Fig. 7 Malignant peripheral nerve sheath tumor extending through femoral canal in 36-year-old man. A, Axial contrast-enhanced CT image shows bulky mass (asterisks) in pelvis extending into anteromedial aspect of thigh bilaterally. Femoral artery (solid arrows) and vein (dashed arrows) are shifted laterally. Tumor extends into thigh through femoral duct. Destruction of pubis (star) is evident. B, CT image with normal findings obtained at same level in 49-year-old man for comparison. B 750 AJR:194, March 2010

6 Imaging of Soft-Tissue Tumor Extension Fig. 8 Myositis ossificans of iliopsoas muscle in 10-year-old boy. Axial T2- weighted MR image shows that soft-tissue tumor (asterisk) extends through muscular lacuna into anterior aspect of thigh. Axial CT image (not shown) indicated calcification in tumor. Femoral artery (solid arrow) and vein (dashed arrow) are shifted medially. A Fig. 9 Pelvic outlet in 49-year-old man. Floor of pelvis is covered by levator ani (arrow) and coccygeal muscles. Tumor in pelvis extends into perineum through gap between these two muscles or may invade these muscles. Asterisk = rectum, star = urinary bladder. Fig. 10 Malignant yolk sac tumor extending through pelvic floor in 20-year-old woman. This case of epithelial tumor was not included in our series. A, Axial T2-weighted MR image shows tumor (asterisk) in pelvis, with heterogeneous high signal intensity. Tumor extends into left side of perineum. Rectum (star) is shifted toward right side. B, Sagittal T2-weighted MR image shows tumor (asterisk) occupying caudal aspect of pelvis. B AJR:194, March

7 Sugawara et al. Fig. 11 Drawing shows inguinal canal is bounded by abdominal wall muscle, fascia, and inguinal ligament. Spermatic cord or round ligament of uterus passes through this canal, and tumor in pelvis extends into scrotum or into large pudendal lip through inguinal canal. A Fig. 12 Liposarcoma involving scrotum, inguinal canal, and pelvis in 71-year-old man. A, Coronal T2-weighted MR image shows scrotum is swollen because of tumor containing fat element (star). Tumor extends into pelvis through left inguinal canal (arrows). B, Contrast-enhanced CT image with coronal reconstruction shows fat density area (asterisk) on left side of pelvis. B 752 AJR:194, March 2010

8 Imaging of Soft-Tissue Tumor Extension A Fig. 13 Plexiform neurofibroma extending along sciatic nerve in 18-year-old man with neurofibromatosis type 1. A, T2-weighted MR image shows that tumor (asterisks) involves spinal canal, pelvis, and gluteal region. Tumor has high signal intensity on T2-weighted image. Tumor extension through greater sciatic foramen is evident (arrow). Tumor also extends into spinal canal through anterior sacral foramen (star). B, Axial T2-weighted MR image obtained at same level with normal findings in 19-year-old man for comparison. Fig. 14 Transosseous extension of hibernoma in 53-year-old woman. Axial unenhanced CT image shows fat-containing tumor (asterisk) in gluteal region extending through ilium (arrow). At 18 F-FDG PET (not shown), extremely increased uptake, consistent with hibernoma, was seen. B AJR:194, March