The Journal of Bone and Joint Surgery (American) 81:882-92 (1999)
© 1999 The Journal of Bone and Joint Surgery, Inc.
Instructional Course Lecture |
Instructional Course Lectures, The American Academy of Orthopaedic Surgeons - New Developments in the Staging and Imaging of Soft-Tissue Sarcomas*
EDWARD Y. CHENG, M.D. and
ROBY C. THOMPSON, JR., M.D., MINNEAPOLIS, MINNESOTA
An Instructional Course Lecture, American Academy of Orthopaedic Surgeons
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Introduction
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New developments in staging have given greater importance to the imaging of soft-tissue sarcomas since the time of the last articles on soft-tissue tumors in the Instructional Course Lectures9,19 or even more recent reviews37. Whereas previous articles have focused on the diagnosis, treatment, and molecular biology of benign19 and malignant9 soft-tissue tumors, the current article will present a new modification of the staging system that has been proposed by the American Joint Committee on Cancer38. Imaging techniques and unique characteristics of soft-tissue tumors will be discussed in order to demonstrate how they are related to the new criteria for staging.
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Historical Development of Staging Systems
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The main purpose of staging a tumor is to determine a patient's prognosis and to help to direct treatment. Malignant tumors have been described as having a life cycle. Therefore, staging identifies specific time-points in a tumor's life cycle (Fig. 1). Staging is usually done at the time that a malignant tumor is diagnosed, but restaging may be performed if the disease progresses and the patient becomes a candidate for various treatment protocols or other clinical research trials46. Pathological criteria, such as the histological grade, amount of necrosis, and size of the tumor as determined at the time of excision, are commonly used for the staging of carcinomas of the skin, bowel, prostate, cervix, and so on. However, in the case of soft-tissue sarcomas, the initiation of treatment such as chemotherapy or radiation before the tumor is excised may alter such factors as the size of the tumor and the amount of necrosis, thus reducing the accuracy of pathological staging that is based on the resected tumor. Therefore, staging based on the pathological characteristics of the resected tumor has given way to staging based on both clinical factors (such as the size and anatomical location of the tumor and the presence or absence of metastatic disease) at the time of the diagnosis and the grade of the tumor as determined on the basis of a biopsy specimen. Both the inaccuracy of staging based on the pathological features of an excised tumor after neoadjuvant treatment and the importance of the grade of the tumor as a prognostic factor increase the value of the biopsy procedure, which is the only opportunity for obtaining fresh, representative tissue for analysis. The biopsy remains a critical procedure in the staging process.
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Fig. 1 Schematic diagram showing the life cycle of a tumor. (Reprinted,
with permission, from: American Joint Committee on Cancer and TNM Committee
of the International Union Against Cancer: Handbook for Staging of Cancer.
From the Manual for Staging of Cancer, Fourth Edition, p. 4. Edited by O.
H. Beahrs, D. E. Henson, R. V. P. Hutter, and B. J. Kennedy. Philadelphia,
J. B. Lippincott, 1993.)
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Although most soft-tissue sarcomas may be grouped together for the purpose of staging, different histological types may have different and unique prognostic factors24. There is general agreement7,10,20,21,30,42 that the size (p = 0.018)42, histological grade (p = 0.001)42, and anatomical location (p = 0.02)30 of the tumor are all independently significant prognostic factors. The size of the tumor in terms of its largest diameter is widely accepted as a prognostic factor7,10,20,21,30,42. While volume is a more accurate indicator of size, diameter is more readily measured and, currently, is a more practical parameter.
The histological grade of the tumor is determined with use of the classic criteria of pleomorphism, cellularity, presence of mitosis, and nuclear atypia, as described in 1939 by Broders et al.6. In addition, some pathologists consider the presence of necrosis to indicate a high-grade tumor4,11. The histological grade has been considered an important prognostic factor by most authors20,21,32,39; however, there is no uniform agreement among pathologists with regard to a scheme for grading. Two, three, and four-tiered grading systems have been advocated by different pathologists4,11,34. As the stratification of the grading increases, the ability to assign grades in a reproducible fashion becomes more difficult. Extension of the tumor into adjacent tissues or anatomical compartments is also considered a prognostic factor16, although recently this has been disputed40.
The anatomical location of the sarcoma has also been shown to be related to the outcome of treatment16,22. A tumor beneath the deep muscle fascia is associated with a poorer prognosis than is a tumor that is superficial to the fascia. Whether this is related to a treatment factor such as the ability to resect the tumor or to the true biological character of the tumor is unknown.
Treatment-related factors such as the margin of resection11,42,48, local recurrence10,14,17,47,50, and adjuvant radiation or chemotherapy have been associated with survival outcome but are not useful for staging as the assignment of stage is independent of treatment modalities. Molecular markers are currently being investigated but, although there have been sporadic reports of their prognostic importance, the most important factors have not yet been identified9,25.
Factors such as age and gender have not been demonstrated to be consistently related to patient survival. However, soft-tissue tumors in children have been staged with use of a variety of systems developed by different study groups and at different treatment centers18,36,37. Historically, the staging of soft-tissue sarcomas in children has been confusing because common solid tumors in children, such as Wilms tumor, neuroblastoma, and rhabdomyosarcoma, have been grouped together. In addition, the common prognostic factors included the feasibility of excision of the tumor as well as the presence or absence of metastasis. The advent of chemotherapy administered both preoperatively and postoperatively, with or without radiation, has raised a valid concern about the importance of the feasibility of excision of the tumor in contrast to the factors of size and anatomical location of the tumor, the age of the child, and the histological diagnosis. For example, neonatal fibrosarcoma is associated with an extremely high rate of cure13, and rhabdomyosarcomas of the head, neck, and genitourinary tract are associated with better prognoses than are tumors with a similar histological grade that are located in an extremity or the trunk51. The prognostic factors for synovial sarcomas in adolescents are similar to those for soft-tissue sarcomas in adults.
Several systems for the staging of soft-tissue sarcomas in children have been proposed, but none has been universally accepted18, although the latest effort51 shows promise. In the meantime, each report on soft-tissue sarcoma in children requires a review of the staging for that series, which makes comparisons with other series difficult. Fortunately, most of these children have a remarkably good outcome, given current protocols for achieving a disease-free state that combine chemotherapy with radiation and excision of the tumor. The five-year survival rate for children who have a conventional soft-tissue sarcoma such as synovial sarcoma in the absence of disseminated disease with bone-marrow involvement or visceral metastasis was most recently reported to be high as 74 percent (twenty-three of thirty-one patients) by the German Cooperative Group29. We currently stage soft-tissue sarcomas in children with the same approach that has been described for adults, with the expectation that, as new outcomes are defined with prospective staging, a better stratification of prognosis will emerge.
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Staging System of the Musculoskeletal Tumor Society
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The system of the Musculoskeletal Tumor Society was proposed for the staging of both bone and soft-tissue tumors in 1980, by Enneking et al.15, and it has gained popularity because it is easy to use and practical. The histological grade is limited to two levels, and the size of the tumor is assessed according to whether or not it is contained within an anatomical compartment. This staging system is based on the principle that tumors grow along the path of least resistance. Although the system is quite functional, it is used chiefly by orthopaedic oncologists; the staging system of the American Joint Committee on Cancer2 is more widely used in studies in the literature on soft-tissue sarcomas.
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Staging System of the American Joint Committee on Cancer
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The staging system of the American Joint Committee on Cancer (Table I) is based on the concept that tumors with similar histological characteristics have similar patterns of growth, and it is generally accepted for the staging of many types of solid malignant tumors2. It is based on the TNM system that was established by the TNM Committee of the International Union Against Cancer, and it focuses on three main events in the life cycle of a tumor: growth, as manifested by the size of the tumor (T); spread to the lymph nodes (N); and distant metastasis (M). Although carcinomas commonly spread to the lymph nodes, sarcomas infrequently do so and therefore this factor is not germane. In the original classification scheme of the American Joint Committee on Cancer2, the size and grade of the tumor were the chief determinants of the stage in the absence of metastasis. A three-tiered grading system is used to distinguish among low, intermediate, and high-grade tumors. However, pathologists have had difficulty differentiating intermediate from high-grade tumors, and the intraobserver and interobserver variation with regard to the assignment of grade has been a disadvantage of this system.
The most recent modification of this classification system was reported in 1997 (Table II)3 and includes two major changes to the previous system. The first change is the introduction of a new parameter: that of anatomical location, or depth, which refers to either a superficial or a deep location of the tumor relative to the investing muscle fascia. The second change is a reduction in the number of grades, from three (low, intermediate, and high) to two (low and high). Although four grades are mentioned in the revised staging manual, the division is only between grade I/II (low) and grade III/IV (high). The grade is determined according to the number of mitotic figures, cytological atypia, and the extent of necrosis6,11. Low-grade tumors have a lower likelihood of metastatic spread than do high-grade tumors. The reduction from three to two grades in the revised staging system is likely to enhance both reliability and reproducibility. Another, minor change is the elimination of the designations of A and B for stage-III lesions. Instead, stage III is reserved solely for the worst tumors (those that are high-grade, large, and deep), and a new subclassification (stage IIC) is used for high-grade, large, superficial tumors. When this revised system is applied to a tumor referral center database encompassing 1019 cases of primary soft-tissue sarcoma, the difference in survival outcomes is quite apparent, with disease-free survival rates, at five years, of 77.9, 63.6, and 36.3 percent for stages I, II, and III, respectively (Table III)3. Similarly, the overall survival rate was different for each stage, as shown with use of life-table survival curves (Fig. 2). This demonstrates the ability of the revised staging system to stratify patients into different prognostic groups.
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Fig. 2 Life-table survival curves for patients who had a soft-tissue
sarcoma, stratified according to the 1997 modified staging system of the
American Joint Committee on Cancer. (Reprinted, with permission, from:
American Joint Committee on Cancer: AJCC Cancer Staging Manual, edited by
I. D. Fleming, J. S. Cooper, D. E. Henson, R. V. P. Hutter, B. J. Kennedy,
G. P. Murphy, B. O'Sullivan, L. H. Sobin, and J. W. Yarbro. Ed. 5, p. 153.
Philadelphia, Lippincott-Raven, 1997.)
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Illustrative Cases
A forty-two-year-old man was seen because of a large tumor in the forearm (Figs. 3-A, 3-B, and 3-C). Both magnetic resonance imaging and pathological examination revealed that the tumor had a maximum diameter of seventeen centimeters. Histologically, the lesion was classified as a low-grade soft-tissue sarcoma. Another patient, a twenty-five-year-old man, had a low-grade fibrosarcoma of the anterior aspect of the proximal part of the thigh (Fig. 4). The tumor was large, subfascial in origin, and extended into the anterior and medial compartments. According to the 1993 staging system of the American Joint Committee on Cancer2, both of these tumors would be classified as stage IB and would be associated with a similar prognosis as they are low-grade lesions that are greater than five centimeters in the largest diameter. However, according to the 1997 modified staging system3, a distinction is made between the two lesions. The tumor in the forearm would be classified as stage IB because of its low grade, its size of greater than five centimeters, and its superficial location, whereas the tumor in the thigh would be considered stage IIA because of its low grade, its size of greater than five centimeters, and its deep location. This portends different prognoses for these two patients. The patient who had the stage-IIA sarcoma in the thigh had metastasis and died of the disease, whereas the patient who had the stage-IB sarcoma in the forearm remained alive and disease-free at the time of writing.
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Figs. 3-A, 3-B, and 3-C: A forty-two-year-old man who had a soft-tissue sarcoma of the forearm.
Fig. 3-A: Clinical photograph.
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Fig. 3-C: Sagittal T1-weighted magnetic resonance image clearly showing the location of the tumor (arrows) to be superficial despite its large size. This was consistent with the intraoperative findings.
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Fig. 4 Axial T2-weighted magnetic resonance image of a low-grade fibrosarcoma (arrows) extending into the anterior and medial compartments of the thigh. The contralateral, normal thigh is shown on the right for the purpose of comparison.
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A sixty-four-year-old woman was seen because of a high-grade undifferentiated sarcoma of the forearm (Figs. 5-A, 5-B, and 5-C). Magnetic resonance imaging clearly demonstrated the subfascial origin of the tumor in the flexor muscle mass, and the axial T1-weighted image showed areas of heterogeneity that represented necrotic regions. The lesion was stage III according to the 1997 modified staging system and was associated with a poorer prognosis. Pulmonary metastasis developed one year after excision of the tumor.
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Figs. 5-A, 5-B, and 5-C: A sixty-four-year-old woman who had a high-grade undifferentiated sarcoma of the forearm.
Fig. 5-A: Clinical photograph.
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Fig. 5-B Axial (Fig. 5-B) and coronal (Fig. 5-C) T1-weighted magnetic resonance images showing regions of varying signal intensity in the tumor (arrow), representing areas of necrosis.
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Fig. 5-C Axial (Fig. 5-B) and coronal (Fig. 5-C) T1-weighted magnetic resonance images showing regions of varying signal intensity in the tumor (arrow), representing areas of necrosis.
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Imaging
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Improvements in high-resolution imaging techniques have allowed oncologists to accurately assess the size, extent, and location of tumors. With the introduction of the depth of the tumor as a major prognostic variable for staging, the importance of imaging becomes paramount as it is the only means of assessing depth accurately before the initiation of adjuvant treatment, operative excision, or entry into a treatment protocol.
Even the most astute examiner is not always able to distinguish between a superficial and a deep tumor as reliably as cross-sectional imaging. The other goals of imaging include screening, detection, determination of the anatomical extent of the tumor, characterization of the tissue type, assessment of the response to treatment, and surveillance during the period following treatment23. Knowledge of the nuances of each imaging modality is essential in order to stage a tumor in the most cost-effective manner.
Radiography
Plain radiographs should be made when a soft-tissue mass is large, is clearly below the deep fascia, or appears fixed to skeletal structures, as important diagnostic clues may be found. Although the detection of a soft-tissue density or shadow is not that useful, the identification of soft-tissue calcifications, ossification, or osseous erosion may provide valuable information for the differential diagnosis. Calcifications resembling phleboliths are commonly seen in hemangiomas. Irregular calcifications may be seen in some soft-tissue sarcomas such as synovial sarcoma and liposarcoma. Soft-tissue ossification can be differentiated from calcification as ossification has the same opacity as bone whereas calcification frequently has more mineralization and is more opaque. Ossification is seen in myositis ossifications and heterotopic bone formation.
Magnetic Resonance Imaging
In most instances, magnetic resonance imaging is the best modality available for detection of soft-tissue tumors, determination of their anatomical extent and depth, characterization, and surveillance. This modality is especially valuable for evaluation of tumors of the extremities and less useful for assessment of lesions of the trunk or the retroperitoneum. In the abdominal and retroperitoneal regions, computed tomography and magnetic resonance imaging are complementary. Computed tomography performed with use of a contrast agent within the gastrointestinal tract is useful for differentiating the bowel from a neoplasm, while magnetic resonance imaging is superior for differentiating muscle, such as the psoas muscle, from neoplastic tissue.
A common error is to assume that a mass that is well circumscribed with a smooth border is benign while one with an irregular margin is malignant. Contrary to intuition, sarcomas tend to grow in a centripetal fashion along the path of least resistance, and a smooth margin between the tumor and the surrounding tissue is usually seen. Infections and posttraumatic conditions frequently have an ill defined border with surrounding edema.
Magnetic resonance imaging is of limited use for distinguishing benign from malignant lesions. Both types of lesions are visualized as nonspecific masses that brighten on T2-weighted and STIR (short-tau-inversion-recovery) sequences.
Certain lesions have a characteristic appearance, which can facilitate diagnosis. Hemangiomas have a variegated, serpiginous appearance due to grapelike clusters of blood vessels (Figs. 6-A and 6-B). Lipomas are composed of normal fat tissue and thus should be isointense with the surrounding fat tissue on all imaging sequences. Popliteal and synovial cysts as well as ganglions are filled with hyaluronic-acid-rich synovial fluid, which is extremely bright on T2-weighted and STIR sequences, and these lesions are homogeneous in appearance. Tumors such as fibromatosis (Fig. 7) and pigmented villonodular synovitis (Figs. 8-A and 8-B) typically have a dark appearance on both T1 and T2-weighted sequences because of the low water of fat content of fibrous tissue as well as hemosiderin deposition, which may provide a presumptive but not a definitive diagnosis. Vascular aneurysms may be seen in continuity with an adjacent artery, and occasionally a mass may be seen in continuity with a major nerve, indicating a tumor of neural origin such as a schwannoma (Figs. 9-A and 9-B).
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Figs. 6-A and 6-B: An intramuscular hemangioma of the lower extremity.
Fig. 6-A: Intraoperative photograph showing dilated venous sacs (arrow) within fatty tissue.
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Fig. 6-B Coronal T2-weighted magnetic resonance image showing the grapelike appearance of the clusters of venous sacs (arrows).
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Fig. 7 Sagittal T1-weighted magnetic resonance image showing a fibromatosis (large arrows) of the antecubital fossa. Note the dark appearance (small arrow) due to the low water or fat content of the fibrous tissue.
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Figs. 8-A and 8-B: Pigmented villonodular synovitis of the knee.
Fig. 8-A: Coronal T1-weighted magnetic resonance image showing the synovitis (arrows) extending proximally into the suprapatellar pouch and the thigh.
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Fig. 8-B Intraoperative photograph of the distal part of the femur and knee, seen through an anterior quadriceps-splitting knee incision, showing darkly stained pigmented tissue (P) due to hemosiderin deposition. S = synovial tissue and F = femoral condyle.
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Figs. 9-A and 9-B: A schwannoma of the distal aspect of the leg.
Fig. 9-A: Coronal T2-weighted magnetic resonance image showing a small, bright tumor mass (arrow) in continuity with the tibial nerve in the leg.
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Fig. 9-B Intraoperative photograph showing the lesion (at the end of the forceps) after excision from the tibial nerve (above the end of the clamp).
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Given the importance of the depth of the tumor as a prognostic factor in staging, magnetic resonance imaging is indispensable. In addition to revealing the size and depth of the tumor, the image can serve as an operative map or an anatomical atlas, helping the surgeon to prepare for the eventual resection of the tumor by aiding in the planning of both the operative approach and the biopsy route. The relationship of the lesion to the surrounding neurovascular structures is delineated in detail. The size of the tumor can be measured both before and after preoperative treatment in order to assess the response to that treatment or progression despite it. The depth of the tumor and the relationship to the investing muscle fascia are seen better with magnetic resonance imaging than with computed tomography or other modalities.
Computed Tomography
Computed tomography is superior to both magnetic resonance imaging and radiography of the chest for the detection of pulmonary metastases. It also is generally preferable to magnetic resonance imaging for the visualization of abdominal, pelvic, and retroperitoneal tumors because structures are more clearly defined, with around ferrous metal implants since it can isolate the metal artifact.
Angiography
Arteriograms have been reported to provide a good assessment of the response to treatment at centers where intra-arterial isolated limb-perfusion chemotherapy is performed27. Otherwise, vascular imaging is not usually necessary as magnetic resonance imaging is sufficient to define any vascular involvement or to localize the displacement of vessels secondary to the mass effect. Occasionally, venous thrombosis can be seen within a dilated major vein, and ultrasound can then be used to confirm the presence or absence of a clot.
Ultrasound
This modality has the advantages of being relatively simple, noninvasive, and quick. It is useful for discerning whether a mass is composed of solid or liquid elements. It is used frequently for the visualization of popliteal masses, when it is important to differentiate popliteal synovial cysts from neoplasms. When a true aneurysm or a pseudoaneurysm is suspected, ultrasound is the imaging method of choice. With the exception of these instances, ultrasound is not widely used for the evaluation of soft-tissue masses.
Scintigraphy
Soft-tissue sarcomas may exhibit some activity on technetium-99 bone-scanning. Generally, bone scans are useful only for evaluating the presence of osseous erosion by an adjacent soft-tissue mass when it is not readily apparent on radiography or computed tomography. Scintigraphy is neither as sensitive nor as specific as magnetic resonance imaging for the detection of soft-tissue masses. However, magnetic resonance imaging can be used to evaluate a local site only, whereas scintigraphy can readily provide images of the entire body when necessary. Scintigraphy is indicated mainly when there is a suspicion of occult metastasis, multicentric disease, or liposarcoma (which is more often associated with nonpulmonary metastasis8 than are other sarcomas). In these unusual situations, gallium scans are more likely to show activity of soft-tissue tumors than is computed tomography or magnetic resonance imaging, neither of which can provide images of the entire body readily.
Magnetic Resonance Spectroscopy
Magnetic resonance spectroscopy is a technique that may have great potential in the future. Although the use of magnetic resonance imaging has become widespread in the past decade, magnetic resonance spectroscopy actually preceded magnetic resonance imaging1. Magnetic resonance spectography can be used to study biochemical changes in tissue in vivo, in a noninvasive manner. It therefore may be an ideal means for studying the metabolic state of a tumor. Indeed, musculoskeletal neoplasms are among the lesions that have been the focus of this research. Phosphorus-31 has been used most commonly for magnetic resonance spectroscopy of sarcomas. Recent reports have addressed the use of metabolic determinations with phosphorus-31 magnetic resonance spectroscopy as indicators of prognosis31,35,44,45,52.
Other potential uses of magnetic resonance spectroscopy are the evaluation of the response of the tumor to therapy on the basis of changes between pretreatment and posttreatment studies and the monitoring of pH values12,28,33,38,41. Problems such as heterogeneity within the same tumor26,43 and the lack of data for the comparison of normal and disease states5 have made evaluation difficult. Therefore, magnetic resonance spectography has not achieved acceptance in routine clinical practice and remains primarily a research tool.
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Overview
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A new modification of the widely used American Joint Committee on Cancer system for staging of soft-tissue sarcomas has been presented. The two major changes are the addition of the depth of the tumor as a prognostic variable and the reduction in the number of tumor grades from three to two. The use of the depth of the tumor for staging places new emphasis on the proper imaging of these lesions, as imaging is the only means for assessing depth before preoperative therapy or operative excision. Magnetic resonance imaging is the mainstay of imaging techniques for most of these lesions, with other modalities having unique advantages in specific situations only.
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Footnotes
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*Printed with permission of the American Academy of Orthopaedic Surgeons. This article will appear in Instructional Course Lectures, Volume 49, American Academy of Orthopaedic Surgeons, Rosemont, Illinois, March 2000.
 No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. No funds were received in support of this study.
Department of Orthopaedic Surgery and Cancer Center, University of Minnesota, 420 Delaware Street S.E., Minneapolis, Minnesota 55455. E-mail address for Dr. Cheng: cheng002@tc.umn.edu. E-mail address for Dr. Thompson: thomp004@tc.umn.edu. Please address requests for reprints to Dr. Cheng.
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