William Fisher Enneking (Fig 1) was born in Madison, WI in May 1926. He earned his BS and MD degrees at the University of Wisconsin in 1946 and 1949, respectively. He served in the US Navy during World War II (1943–1944) and again during the Korean War from 1950 to 1962. His career in orthopaedics started with his residency at the University of Chicago (1952–1955). A year later, he became Chief of Orthopaedics at the University of Mississippi and in 1960, he became Chief of Orthopaedics at the University of Florida in Gainesville. Enneking has published numerous papers on musculoskeletal oncology including this classic article, which defines a system for surgical staging of musculoskeletal sarcomas. He was the first President of the Musculoskeletal Tumor Society and is the recipient of numerous honors awarded for his research and teaching. In 1963, Enneking was President of the Orthopaedic Research Society; in 1980, he was President of the American Board of Orthopaedic Surgery; and in 1984, he was President of the American Orthopaedic Association.Fig 1: Dr. William Fisher EnnekingHistorically, an adequate surgical procedure has been the most effective means of treating the majority of primary musculoskeletal sarcomas, and amputation has figured prominently in the surgical armamentarium. 4,7,9,19,21,29,41 The recent evidence that certain chemotherapeutic agents may have significant anti-sarcoma activity 2,15,17,38 and coincident technical advances in irradiation therapy, radiographic localization, and reconstructive surgery have fostered enthusiastic interest in extremity-saving treatments. Almost all such treatments emphasize limb salvage as an alternative to amputation and are usually performed under a protective cloak of adjunctive chemotherapy, irradiation or immunoactive agents. 20,23,24,30,37,39 Since neither chemotherapy nor irradiation therapy alone has been shown to assure long-term local control of bulk disease, surgical intervention remains an essential step in the overall management of musculoskeletal sarcomas. 3,9,17,18,29 Questions concerning the magnitude and timing of the surgical procedure are as unanswered as those relating to the most appropriate use of the adjuncts themselves. Increasingly, the surgeon and his patient are confronted with a bewildering array of therapeutic options, the long-term outcomes of which are unknown. These relatively rare sarcomas increasingly are distributed among a variety of treatment protocols in which multiple parameters differ. This trend necessitates interinstitutional cooperation if sufficient numbers of patients are to be available for the timely evaluation of treatments in clinical use. Such cooperation and even effective interinstitutional communication are seriously hampered by the lack of uniform language, so that meaningful comparison of treatments is currently impossible. Prime factors include the lack of a consistent definition of the surgery performed and a serviceable surgical staging system encompassing bone and soft tissue. Standard terminology will assure that like and unlike treatments are appropriately compared. Although an effective staging system should serve all members of the multidisciplinary team, the biologic behavior of musculoskeletal sarcomas suggests that the most useful staging system will articulate with the surgical procedure. SURGICAL STAGING A surgical staging system for sarcoma should: Incorporate the most significant prognostic factors into a system which describes progressive degrees of risk to which a patient is subject. Delineate progressive stages of disease that have specific implications for surgical management. Provide guidelines to the use of adjunctive therapies. Since its organization in 1959, the American Joint Committee for Cancer Staging and End Results Reporting (AJC) has undertaken responsibility for developing clinically useful staging systems for many kinds of cancer. The intent of staging is to designate “the state of a cancer at various points in time and is related to the natural course of this particular type of cancer.” The purpose is to: “provide a way by which this information can be readily communicated to others; to assist in decisions regarding treatment; and to be a factor in judgement as to prognosis. Ultimately, it provides a mechanism for comparing like or unlike groups of cases, particularly in regard to the results of different therapeutic procedures.” The AJC philosophy expresses the idea that “for most types of cancer, the extent to which the disease has spread is probably the most important factor determining prognosis and must be given prime consideration in evaluating and comparing different therapeutic regimens.” To this end, the TNM system, where T designates the local extent of disease (often translated into size) of the primary tumor, N designates nodal extent, and M, metastatic extent, has been consistently used. 22,31 In addition to anatomic extent, the histopathologic analysis and grade of the tumor are other recognized prime determinants. 6,13,14,16,19,22,26,27,28,31–33 The single attempt to develop a staging system for sarcomas of bone by the Task Force on Malignant Bone Tumors of the AJC failed to yield a satisfactory system. They recommended that institutions with access to large numbers of patients, consistency in management, and long-term follow-up undertake this task. 11 The staging system for soft tissue sarcomas proposed by the AJC in 1977 31 and the recent modification suggested by Hajdu 16 have, in our experience, been of limited value in the surgical management of soft-tissue lesions. 12,13,37 A surgical staging system for musculoskeletal sarcomas is most logically accomplished by assessment of the surgical grade (G), the local extent (T), and the presence or absence of regional or distant metastases (M). The sarcomas for which this system was designed are those arising from the mesenchymal connective tissue of the musculoskeletal system. Lesions derived from the marrow, reticuloendothelial tissue housed within bone and mesenchymal soft tissue, and the skull are not included in this system because their natural history, surgical management, and response to treatment are quite different. Thus, leukemias, plasmacytoma, lymphomas, Ewing’s sarcoma, undifferentiated round-cell lesions, and metastatic carcinomas are excluded. Surgical Grade (G) From the standpoint of surgical planning, neoplasms of any histogenesis are divided into two grades: low (G1) and high (G2). The majority of low-grade lesions may be managed with relatively conservative procedures while the high-grade lesions require more aggressive procedures to achieve the primary goal of a definitive oncologic surgical procedure—local control. 12,13,28,29 In general, low-grade lesions correspond to Broder’s I or II and have a low risk for metastases (<25%). Histologically, they are well-differentiated, have few mitoses, and moderate cytologic atypia. Their clinical course is marked by indolence. When they occur in bone, there is a tendency toward circumscription by reactive new bone. High-grade lesions (Broder’s III and IV) have a significantly higher incidence of metastases. They are characterized by poor differentiation, a high cell/matrix ratio, a high mitotic rate, necrosis, and microvascular invasion. Their clinical course is correspondingly marked by activity. Radiographically, the bone primaries are poorly marginated and have a permeated pattern. Angiographically, a reactive neovasculature usually rims the lesion. The surgical grade may differ slightly from the purely histologic grade by consideration of clinical and radiographic features. Thus, the surgical grade may be weighted by the radiographic characteristics in chondrosarcoma, by the histologic appearance in fibrosarcoma, or by the clinical course in giant-cell tumor of bone. Usually there is good correspondence among the clinical, radiologic, and histologic findings. The surgical grades (G) of a number of musculoskeletal sarcomas are given in Table 1. Each lesion ultimately is assessed on its own clinicopathologic features; not all parosteal osteosarcomas are low-grade, 1 nor are all intraosseous osteosarcomas high-grade. 40 In the absence of metastases, this method of separating lesions determines the stage: Stage I = G1; Stage II = G2. The stage is linked to surgical planning through providing information about what kind of surgical margin is required for definitive local control.TABLE 1: Surgical Grade (G)Surgical Site (T) Just as the surgical grade is a measure of the overall biologic aggressivity of a lesion and indicates what kind of surgical margin is appropriate, 12,13,28,35 the anatomic extent or setting (T) indicates how the surgical procedure is most likely to be achieved 4,5,7,13,21,25,26,33,41 or even whether the desired margin can be achieved at all. The prime factor in determining how a surgical margin is accomplished is whether the lesion is within a well-delineated anatomic compartment or is diffusely infiltrating poorly demarcated adventitial planes and spaces. Therefore, the two stages are subdivided by whether the lesion is intracompartmental (A) or extracompartmental (B). Anatomic compartments have natural barriers to occult tumor extension: in bone, the barriers are cortical bone and articular cartilage; in joints, articular cartilage and joint capsule; and in soft tissues, the major fascial septae and the tendinous origins and insertions of muscles. In contrast, the ill-defined interfascial spaces and planes are limited only by loose areolar tissues that favor occult micro-extension. Because major neurovascular bundles lie in these interfascial extracompartmental tissues, a lesion involving these structures is by definition extracompartmental. Both lesion size and its physical distance from vital structures are related to compartmentalization, but they are not determinants in surgical planning. 33 Although the larger lesions are more likely to become extracompartmental, neither large intracompartmental nor small extracompartmental lesions are unusual. Similarly, a lesion may be separated by only a few millimeters from a major nerve or vessel and yet be contained by a fascial septum that provides an adequate plane of dissection without sacrifice of the adjacent structures. Because satellite micronodules are routinely found in the pseudocapsular and reactive zones about all sarcomas, these zones must be considered an integral part of the lesion. Whether or not the lesion and its reaction is contained within a well-defined anatomic compartment more accurately indicates the feasibility of a local procedure than does the size or proximity to vital structures. 13 The various surgical compartmental sites (T) are listed in Table 2. The the anatomic and The and tissues are as an anatomic compartment because the is a to In the the is a a lesion that has neither the bone nor the is a lesion the bone or it is Surgical anatomic sites are listed in the of Table 2. A lesion is extracompartmental if it in these tissues or if it into from an intracompartmental Thus, a sarcoma arising in the is an of the into the is and a of the bone is extracompartmental. A lesion which the is extracompartmental, as is a lesion it the and intraosseous lesion that from cortical bone or an lesion that a joint is extracompartmental. Surgical of a lesion without of the lesion any tissue planes to the lesion or at risk for Thus, most intracompartmental lesions are to extracompartmental lesions by any surgical which does not the lesion. of and surgical have that a and extracompartmental may be by the appropriate of history, physical and other or The presence or absence of metastases is the major factor related to prognosis and surgical planning. In sarcomas the of to the and the regional to have the prognostic They the of local and the presence of indicates for STAGING on these a Surgical Staging that bone and soft-tissue lesions by grade or anatomic setting or and metastases or has been The stages are of grade and The stages are subdivided into A and the of the lesion. The stages and their are in Table Stage I those low-grade lesions shown in Table 1 Stage the high-grade lesions in Table 1 and Stage III lesions, those with regional or distant metastases or I and II are subdivided by the and extracompartmental shown in Table 2. Thus, Stage is a low-grade, intracompartmental lesion with regional or distant metastases Stage is a low-grade, extracompartmental lesion without metastases Stage is a intracompartmental lesion of metastases Stage is a extracompartmental lesion without metastases and Stage III is of grade and setting with metastases or or Surgical The of the Surgical Staging with surgical planning is accomplished by the to a surgical procedure with that have local types of on the of the surgical margin to the and its are A of these and the disease is in Table Since any of these may be accomplished by a local procedure or an significant surgical procedures These are in Table and margin is accomplished by a procedure in which the dissection within the lesion. or tumor is at the of the and there is of all the tissue local procedures are performed as a by of a or by of a lesion to be managed by other amputation is as a but more is because of occult of the lesion. A margin is achieved by a procedure in which the lesion is in The plane of dissection is through the or reactive tissue about the and performed for lesions, disease at the margin of the in a high of the a local is usually as or of a lesion. amputation is usually as a an definitive procedure by anatomic or as an adjunctive procedure. A margin is accomplished by a procedure in which the its reactive and a of tissue are as a single The plane of dissection is through tissue but within the is to the of from to or bone from joint to The local procedure probably to what is to as local and A margin is definitive surgical management for Stage I lesions and can usually be accomplished by a local procedure for lesions. Because Stage lesions usually of bone, soft and neurovascular amputation is more likely to be A margin is achieved by a procedure in which the reactive and the or bone are as the plane of dissection through or the joint and to the bone and through the tendinous and of muscles. the dissection the major fascial of the soft tissue compartments or the of intraosseous lesions. A margin does not a distance from the lesion to the margin of the than a A margin on the other of the septum of a lesion in the will a margin but may be than a margin achieved by A margin is definitive for Stage II lesions. A local can be for a Stage lesion. a lesion more than or into or in the extracompartmental planes or compartmental is and a margin is usually not with a local procedure. Thus, amputation is usually to achieve a margin in Stage lesions, and it a or amputation to the joint in These various procedures are in 1 and 2. Surgical Surgical 1: The various local procedures are The the plane of dissection and the of tissue to achieve the various procedures for a lesion within the compartment of the types of procedures may be for bone The various types of are shown for a lesion of the types of amputation may be for soft-tissue for a lesion within a single may be a local or a local the the a local the a the a local the is of separated by loose areolar tissue within a large contained compartment such as the is in the but only in the and by a local The and of this surgical staging system has been in two quite different by the University of Florida musculoskeletal oncology and by an interinstitutional by the Musculoskeletal Tumor The evaluation patients on the musculoskeletal oncology at the University of Florida The has patient effective for patient and a well-defined surgical A of primary have been and is in and have been to have been and the of new The surgical and stage for surgical planning. The stage was of the surgical the of the evaluation of the staging system. The evaluation of the system was among 13 institutions University of University of for University of University of and of of the are with in the management of musculoskeletal The of their surgical from conservative to These 13 institutions have their own of follow-up and for and a of the of musculoskeletal surgical oncology as it Each was a with a of the staging system University of and to stage and of musculoskeletal sarcoma The only that the have a follow-up be without regard for This in the system was in of cases, all related to from analysis because of and in of the The Because of the limited of in the the by the method of for The by the method of and by numbers of patients at risk for the time The for the is shown in Table and the by stage in Table The is to other large with the of the of is a of bone lesions and a of high-grade by Surgical Stage = of as a of stage for the and is in The of by method for the is different from that of the it whether the analysis is or on This to the that analysis of provides a satisfactory of the of and the of for The of for the (A) and as as the for the is shown by stages for a of as a of stage for the of of bone and soft-tissue sarcomas is shown in year of there is a significant the of for stage with Stage I lesions are at low risk and differ from those with Stage II lesions The and lesions is not with Stage II lesions are at high risk The Stage and is significant The of by the various stages a separated to bone = or soft = The of as a of stage for of these primary sites is in is in the of bone and soft tissue lesions that are of The of by stages a bone and soft-tissue and AJC systems for soft-tissue lesions compared. The interinstitutional not sufficient information to stage their soft-tissue lesions by the AJC and the from the The results of comparing soft-tissue primary lesions are shown in From to AJC and are AJC and are to Stage The AJC is to AJC and have at all of and their is not they are to Stage The AJC is to Stage The incidence of by stages a The the lesions by the Surgical Staging while the the lesions by the AJC system for soft-tissue The Surgical Staging in our has the has in surgical planning and of lesions in such a way that meaningful may be various treatment The purpose of this is not to what an appropriate surgical procedure in a given the purpose is to that in the of surgical the surgeon must two is local control of the lesion and the other is of The Surgical Staging on the of the risk factors with various surgical treatment planning by the of alternative surgical in which the risk of for a given surgical procedure may be the of by The and with the purpose of the procedure the the of effective adjunctive therapy, and other to the of The is In to different of surgical the stage of the disease and adjunctive therapy must be the In to the of the stage and the surgical procedure must be the is to the of chemotherapy two patients with Stage has a local and the other a is to the of irradiation therapy in sarcoma patient a Stage lesion with a local and the other a Stage lesion with a local Since the definitive surgical procedure is the single most important therapeutic it and the stage of the lesion must be in to the of The AJC system is a system with The system is on assessment of histologic grade or size or in cases, regional or distant or and by the proximity of the lesion to neurovascular structures and bone. Although it has the of into that histologic grade is a prime factor in the assessment of risk in sarcoma, the a number of that its clinical use of the which their in the and or other These lesions such a different and that they should not be with lesions of the for The of sarcomas into histologic grades is a histologic Although it is likely to have to the it has to the surgeon in of surgical because there is surgical procedure. The T is by lesion that lesion size has prognostic that is a of anatomic rate, and time to Since neither nor time to can be this in the AJC system have more if it the extent by anatomic compartmental The is more consistent with the natural biologic behavior of the sarcomas, and has for the to Stage III as are lesions with regional metastases. is so in the natural of these lesions at the time of as to not be a When this relatively rare does the prognosis is nodal metastases are given with other metastases, the surgeon that a procedure is likely to be or must be with other treatment to be of a major or is poorly and the by which these are to be are not Lesions with such are to a higher stage without regard for of our soft-tissue sarcoma by this method results in these Stage lesions a prognosis to AJC and lesions. Such is a of the anatomic setting of the and as does not require a Lesions of certain histogenesis are to at Stage III because of their poor prognosis. This is a of grade and should be as grades of these lesions and they should be The AJC system proposed for primary bone lesions is so that have not it with the Surgical Staging it is different from the AJC soft tissue system and if require the use of two systems that not comparison bone and soft-tissue sarcomas of the Because definitive surgery is the primary treatment for sarcomas of bone and soft tissue, and because the their biologic behavior and surgical procedures are the for a staging system for groups be more useful than two and different is that the of the staging system proposed recognized by and They divided which they to be of into progressive histologic grades and their with the clinical course and Their clinical of metastases our that a into high and low grade is and sufficient to the risk of distant size was not an important determining factor in but anatomic and of treatment They recognized the histologic grade and an adequate surgical procedure to patient Their that local of the may in a this procedure is by local and in the and II and is a of the of tumor surgery at our They the for adjunctive and to factors in their appropriate use by comparing treatment The in treatment of the in which amputation a of the disease an important in The amputation on the and and on the other is at most is as as it was The Surgical Staging for sarcomas of bone and soft tissues is and has a high of and is to surgical planning and is quite that in comparing treatment protocols the prognostic stage and the extent of the surgical procedure must be and meaningful can be The absence of a staging system with surgical procedures has hampered the of the of various in musculoskeletal sarcomas. The surgical staging system and surgical the for the interinstitutional currently by the Musculoskeletal Tumor A surgical staging system for musculoskeletal sarcomas bone and soft-tissue lesions of any histogenesis by the grade of biologic by the anatomic and by the presence of The and of metastases, are subdivided by whether the lesion is within well-delineated surgical or such compartments in ill-defined fascial planes and spaces. are as and and the surgical margin to the lesions, its reactive and anatomic The system defines significant progressive stages of risk which have surgical When the system is linked to surgical it appropriate evaluation and comparison of the new treatment protocols designed to surgical
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