Classification systems for osteonecrosis: an overview

Orthop Clin N Am 35 (2004) 273 – 283

Classification systems for osteonecrosis: an overview Marvin E. Steinberg, MDa,*, David R. Steinberg, MDa,b a

Department of Orthopaedic Surgery, School of Medicine, University of Pennsylvania, 3400 Spruce Street, Philadelphia, PA, USA b Presbyterian Medical Center, One Cupp Pavilion, 39th and Market Streets, Philadelphia, PA 19104, USA

The management of osteonecrosis remains one of the more perplexing problems facing the orthopedic surgeon. There is much to be learned about the etiology and pathophysiology of this condition. Without specific treatment 80% of clinically diagnosed cases will progress, and most will eventually require arthroplasty [1]. The goal is therefore to diagnose and treat the condition in its earliest stages. A number of surgical procedures have been described to retard or prevent progression and to preserve the femoral head. Although many if not most yield results better than symptomatic treatment alone, none is entirely satisfactory. Because the treatment of osteonecrosis is determined in large part by the stage of the disease, it is important to use a reliable and effective method of classification and staging. In addition, it is extremely difficult to compare one method of treatment with another and to evaluate accurately the results of various studies. This difficulty arises in part because of the many variables used to determine the method of treatment, follow progression or resolution, and evaluate the outcome. Several methods of classification and evaluation have been used, and it is hard to make a correlation between them. Investigators working with osteonecrosis have acknowledged that the uniform use of a single, effective method for staging and evaluation would provide many advantages. It would help clinicians establish a prognosis, follow improvement or progression, compare the effectiveness of different methods of treatment, and determine the best method of management for patients with different stages of

* Corresponding author. E-mail address: [email protected] (M.E. Steinberg).

osteonecrosis. The ideal classification system should correspond closely to the pathologic and radiographic changes that occur in osteonecrosis and should clearly and distinctly characterize each separate stage. It must be quantifiable and allow accurate measurement of the size of the necrotic segment and the extent of joint involvement. The patient’s symptoms and physical findings, although important in management, should not be a part of the classification per se. The system must be objective, relatively simple to use, and reproducible. It should enable the physician to trace the progression from the very earliest to the latest stages. Older, invasive techniques should be avoided. Newer diagnostic modalities, such as MRI, must be included, and the system should leave room for the development of even more sensitive methods of diagnosis and evaluation. Its effectiveness should be established in actual clinical use, and its advantages over other systems should be documented. This article gives an overview of the systems used most frequently for the classification of osteonecrosis so the reader can better understand and compare the outcomes of studies that report their results using different methods of classification. The essential features of an ideal classification or staging system have been outlined to assist the reader in deciding which of the available systems best meets these goals.

Systems for classification and staging In a recent paper, Gordon et al [2] reviewed 109 studies published since 1985 regarding the results of treatment of osteonecrosis. These studies cited 12 major classification systems, 5 of which accounted for approximately 80% of the citations. The classification

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Stage

Clinical features

Radiographic signs

Haemodynamics

Scintigram

Diagnosis without Core Biopsy

0 + +

0 0 Diffuse porosis, sclerosis, or cysts

+ ++ ++

Reduced uptake? Increased uptake +

Impossible Impossible Probable

+ or normal

+

Certain

+

+

Arthritis

Early 0 I II

Preclinical Preradiographic Before flattening of head Or sequestrum formation

Transition

Flattening Crescent sign

Late III

Collapse

++

IV

Osteoarthritis

+++

Broken contour of head Sequestrum Joint space normal Flattened contour Decreased joint space Collapse of head

Data from Ficat RP. Idiopathic bone necrosis of the femoral head: early diagnosis and treatment. J Bone Joint Surg [Br] 1985;67:3 – 9.

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Table 1 Classification of osteonecrosis

M.E. Steinberg, D.R. Steinberg / Orthop Clin N Am 35 (2004) 273–283

system most frequently referred to was that of Ficat and Arlet, followed by those of The University of Pennsylvania, Marcus, Enneking, and Massam, the Association Research Circulation Osseous (ARCO), and the Japanese Investigation Committee. In addition, 10 authors described ancillary methods of evaluating osteonecrosis without incorporating them into a specific staging system. The more commonly used staging systems are described briefly. These are based primarily on the changes seen on radiographs and other imaging studies, although some have included clinical features and pathologic findings. For more detail and for specific instructions as to how the systems may be used, the reader is encouraged to refer to the citations in the bibliography.

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Marcus, Enneking, and Massam In 1973 Marcus, Enneking and Massam [6] described six radiographic stages of osteonecrosis. These stages were correlated with the patient’s symptoms and physical examination, as well as with the gross and histologic findings (Table 2). MRI was not available at this time, and no preradiographic stages were included. It was not always easy to distinguish between stages based upon the authors’ descriptions. No attempt was made to quantitate the extent of involvement. This system was subsequently modified by Urbaniak et al [7] and by Enneking [8] to include MRI and later to include quantitative measurements [9]. Sugioka

Ficat and Arlet Perhaps the first system used for staging osteonecrosis was described in the early 1960s by Arlet and Ficat [3] and included three specific stages. In the 1970s a fourth stage was added [4], and this form is the one most widely used today, although a stage 0 and a transitional stage were added later (Table 1) [5]. The patient’s symptoms and physical findings were in part correlated with the radiographic changes, and both histology and functional evaluation of bone (bone marrow pressure recordings and intramedullary venography) were required in the early stages. Bone scanning or scintigraphy was used, but MRI was not included. A major disadvantage of this classification was that it did not include any measurement of lesion size or articular surface involvement. Thus it could not differentiate between small and large lesions, nor was it a sensitive indicator of progression. The classifications of Ficat and Arlet are frequently modified to include MRI, whereas bone biopsies and functional evaluation of bone are seldom used today.

In 1976 Sugioka [10] reported on the results of his transtrochanteric anterior rotational osteotomy, at which time he categorized hips into four radiologic grades (Table 3). He also described a method for measuring the extent of the lesion as seen on the lateral radiography and expressed this measurement as a percentage of the entire femoral head. He later devised a series of templates that could measure the extent of femoral head flattening and the ratio of necrotic to intact articular surface [11]. This measurement was an important predictor of outcome in hips being considered for rotational osteotomy. His results were closely correlated with both the radiologic stage and with the amount of intact articular surface available for weight bearing after rotation of the femoral head. The location of the lesion also determined whether the surgeon should perform an anterior rotation, which was more common, or posterior rotation, depending on which would better shift an intact articular surface into the region of major weight bearing.

Table 2 Stages of aseptic necrosis (Marcus, Enneking, and Massam) Stage

Clinical signs

Radiographic signs

Pathologic signs

1 2

Asymptomatic Asymptomatic

3

Onset of pain

4

Pain with activity

5

Pain without activity

Areas of infarct and creeping substitution Advancing fibrovascular zone of repair and advanced creeping substitution Subchondral fracture through dead bone, but cartilage intact Fracture through dead bone and cartilage; calcification of necrotic marrow Loose osteochondral fragment

6

Pain at rest

Mottled areas of increased density Infarct demarcated by zone of increased density Subtle flattening, crescent sign (subchondral radiolucency) Clear flattening of femoral head with depression of lateral edge of infarct Flattening and compression of infarct, narrowing of articular cartilage Progressive compression and erosion of head; superimposed degenerative arthritis

Loss of articular cartilage; marked degenerative arthritis

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Table 3 Radiologic grading (Sugioka) Grade

Description

I II III

Necrosis just visible; head still round Flattening of head Markedly collapsed head without joint space narrowing Advanced changes in head with joint space narrowing

IV

University of Pennsylvania The University of Pennsylvania staging system, developed in the early 1980s, identified seven clearly defined radiographic stages, incorporated both Technetium bone scans and MRI, and included specific measurements of lesion size and articular surface involvement. The patient’s symptoms and physical findings were not included as part of the staging but were considered important in determining treatment (Table 4) [12,13]. Perhaps the two most important features of this system are that it was the first to use MRI as a specific modality for determining stage and was the first to include measurement of lesion size and surface involvement as an integral part of the system. Measurements of the same hip made on plain radiographs and on MRI sections were found to be quite similar, and therefore it was decided that MRI would be limited to examining preradiographic hips because it added little to the evaluation of lesions that were well seen on plain radiographs [14,15]. With this system the stage is determined initially based upon the type of changes seen on radiography or MRI. The extent of involvement is then measured or estimated and recorded as mild (A), moderate (B), or severe (C). For routine clinical use, estimation is simple and reasonably accurate; for research purposes the size of the necrotic lesion and the amount of articular involvement should be measured as described [15]. (An alternate method of determining lesion size is by using angular measurements, initially described by Kerboul [16,17]. A small lesion with less than 15% of head involvement (A) corresponds approximately to a combined angle of less than 150°; a moderate lesion (B) corresponds to an angle of 150° to 200°; and a large lesion (C) corresponds to an angle of more than 200°.)

classification [18 – 20]. Hips were initially evaluated by the four-part Ficat and Arlet classification [4]. Stages II and III were further subdivided according to the type and location of the lesion as seen on anteroposterior radiographs (Fig. 1). Stage I and IV hips were not included. Although the system was useful in predicting which hips had a greater chance of collapse, it was found to be less accurate than desired. Accordingly, later investigators suggested that the area of necrosis as seen in both the anteroposterior and lateral projections also be evaluated [19,21]. Other concerns with this system included its ambiguity, the exclusion of stages I and IV, its lack of actual measurement of lesion size, surface involvement, or extent of collapse, and its failure to reflect accurately the pathophysiology of the condition. This system of staging is seldom used outside of Japan.

Table 4 University of Pennsylvania system for staging avascular necrosis Stage Criteria 0

Normal or nondiagnostic radiograph, bone scan, MRI Normal radiographs; abnormal bone scan and/or MRI A – Mild (<15% of femoral head affected) B – Moderate (15% – 30%) C – Severe (> 30%) Cystic and sclerotic changes in femoral head A – Mild (<15% of femoral head affected) B – Moderate (15% – 30%) C – Severe (>30%) Subchondral collapse (crescent sign) without flattening A – Mild (<15% of articular surface) B – Moderate (15% – 30%) C – Severe (>30%) Flattening of femoral head A – Mild (<15% of surface and < 2 mm depression) B – Moderate (15% – 30% of surface and 2 – 4 mm depression) C – Severe (>30% of surface and > 4 mm depression) Joint narrowing or acetabular changes A – Milda B – Moderatea C – Severea Advanced degenerative changes

I

II

III

IV

V

VI a

Japanese Investigation Committee for Avascular Necrosis In 1987 the Japanese Investigation Committee for Avascular Necrosis described a new radiographic

Average of femoral head involvement, as determined in stage IV, and estimated acetabular involvement. From Steinberg ME, Brighton CT, Corces A. Osteonecrosis of the femoral head; results of core depression and grafting with electrical stimulation. Clin Orthop 1989;249:199 – 208; with permission.

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Type 1-A

Type 1-B

Type 1-C

Type 2

Type 3-A

Type 3-B

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Fig. 1. Radiographic classification of avascular necrosis of the femoral head as proposed by the Japanese Investigation Committee for Avascular Necrosis of the Femoral Head. Type 1 is characterized by the presence of a demarcation line in the femoral head and is divided into three subtypes, 1-A, 1-B, and 1-C, according to its relationship to the weight-bearing surface. Type 2 shows early flattening of the weight-bearing surface but has no demarcation line around the necrotic area. Type 3 has cystic lesions and is divided into two subtypes according to their site in the femoral head. (From Ohzono K, Saito M, Sugano N, Takaoka K, Ono K. The fate of nontraumatic avascular necrosis of the femoral head. Clin Orthop 1992;277:73 – 8; with permission.)

Association Research Circulation Osseous

Other methods of evaluation

Realizing the advantages that would result from the use of a uniform system of staging by the international community, ARCO appointed a Committee on Terminology and Staging to establish a uniform terminology, a set of diagnostic criteria, and a classification of osteonecrosis. In 1991 the committee endorsed The University of Pennsylvania staging system [22]. In 1992 localization of the lesion, as described by the Japanese, was added [23,24]. This addition, however, was found to have made the system too complex, and in 1993 stages III and IV, and stages V and VI were combined to provide a total of five rather than seven stages (Fig. 2) [25]. Subsequently, concern was expressed that the system no longer provided a separate category for the hip with a crescent sign without femoral head flattening and that it remained unnecessarily complicated by the inclusion of a separate category for localization, which most investigators do not find useful.

There are other less frequently used methods for staging osteonecrosis. Also, existing systems are frequently modified to bring them up to date, although these changes are not routinely incorporated into the literature. Histologic evaluation has been included as a part of some staging systems, such as those of Massam, Enneking and Marcus [6] and Ficat and Arlet [4,5]. John Paul Jones [26] included both gross and histologic features when he described five stages of the pathophysiology of osteonecrosis. ARCO proposed a simple descriptive histologic classification that was separate from its radiologic classification [22]. There are also several important publications which describe the gross and histologic changes seen in osteonecrosis without attempting to formulate a system of classification. This evaluation requires examination of the entire excised femoral head rather than a small biopsy specimen for a thorough evaluation.

278 M.E. Steinberg, D.R. Steinberg / Orthop Clin N Am 35 (2004) 273–283 Fig. 2. ARCO international classification of osteonecrosis. (From Gardiniers JWM. ARCO Committee on Terminology and Staging. Report on the committee meeting at Santiago de Compostella. ARCO Newsletter 1993;5:79 – 82; with permission.)

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Therefore, from a clinical standpoint it is seldom practical to incorporate histology as a part of staging. MRI is currently the best single method for early diagnosis of avascular necrosis. It is extremely sensitive and specific when used in conjunction with clinical and radiographic evaluation. It is currently an integral part of several staging systems and has also been used by some investigators as a separate tool for classification and for quantification of lesion size [14,27 – 32]. Koo and Kim [33] used MRI to quantify the extent of osteonecrosis of the femoral head using angular measurements on midcoronal and midsagittal T1 images. Their technique is somewhat similar to that used earlier by Kerboul et al [16] on plain radiographs. They used the product of two angular measurements to approximate the relative volume of necrosis in the weight-bearing portion of the femoral head. They found measurements by different observers to be quite consistent and noted a close correlation between this index of necrosis and eventual collapse of the head. They believed that MRI was more sensitive and more accurate than plain radiographs. Other authors, however, have found a close correlation between MRI and radiographs [14,34] and question the need to obtain MRIs of hips in which the lesion is well demonstrated on plain films. Neither MRI nor other currently available imaging techniques will detect all necrotic lesions. It requires approximately 3 weeks after a vascular insult for the development of changes in bone that can be detected by MRI, and very small lesions may go undetected [35]. More sensitive methods for early detection of osteonecrosis may be developed in the future. Therefore some classification systems include a stage 0 to indicate the suspicion of osteonecrosis that cannot be initially confirmed using noninvasive modalities currently available [5,15,25]. Before the development of MRI, radionuclide bone scanning or scintigraphy was an important tool for the early diagnosis and classification of osteonecrosis. This technique is nonspecific and less sensitive than MRI and is infrequently used today. It may play a limited role when MRI is not available or when a single test is desired to rule out the presence of multiple areas of bone involvement [35,36]. CT is infrequently used because of its cost and x-ray exposure. It has a limited role in the evaluation of a patient with osteonecrosis but may enable clinicians to see and measure small areas of femoral head collapse that do not appear on plain radiographs. CT can also be used to help measure the size of the necrotic segment. This measurement may assist in determining prognosis and may influence the method of treatment [37].

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There have been few reports on the use of single photon computerized tomography, positron emission tomography, and gadolinium-enhanced MRI in diagnosing and evaluating osteonecrosis. The role of these studies has not yet been determined, and they are currently not in routine use for this purpose [38 – 40]. Specialized angiographic techniques have also been used to evaluate osteonecrosis. These have documented abnormal vascular patterns in a high percentage of hips. They are invasive studies that require special expertise to perform and interpret. To date, they have been used primarily for purposes of research rather than for clinical diagnosis or evaluation [35,41 – 43]. In 1974 Kerboul et al [16] found that the outcome of proximal femoral osteotomies for osteonecrosis was related to the location and extent of necrosis. The extent of necrosis was determined by measuring the arc of the articular surface overlying the lesion on both anteroposterior and lateral radiographs. These two measurements were added together and have

Fig. 3. Method of measuring lesion size as described by Kerboul, Thomine, Postel, and Merle D’Aubigne. Diagram shows how the extent of the necrosis was recorded. (From Kerboul M, Thomine J, Postel M, Merle D’Aubigne R. The conservative surgical treatment of idiopathic aseptic necrosis of the femoral head. J Bone Joint Surg [Br] 1974;56:291 – 6; with permission.)

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been referred to as the combined necrotic angle (Fig. 3) [17]. The extent of necrosis was considered large if the angle was greater than 200°, medium if the angle is between 160° and 200°, and small if the angle is less than 160°. The location of the necrotic segment was also considered important. When the necrotic segment was located anteriorly, better results could be anticipated than when it extended posteriorly because the flexion-adduction osteotomy would then rotate a normal segment of articular surface into the major weight-bearing region. Wagner and Zeiler [44] and Sugioka et al [11] reported similar observations. In 1995 Koo and Kim [33] used similar angular measurements made on MRIs rather than on radiographs to predict outcome. They used these measurements independently rather than as a part of a comprehensive classification system. Subsequent publications have used angular measurements to estimate lesion size in conjunction with other classification systems [17].

Discussion There is general agreement that the study and treatment of osteonecrosis would benefit greatly if workers in the field could agree upon the use of a single effective system of classification and staging. Until this agreement is reached, it is necessary to understand the various systems in common use to be able to compare the results of studies that use different methods of classification. Because the pathogenesis of osteonecrosis has been reasonably well established, there are certain basic similarities in the various systems of classification. There are, however, considerable differences in the number of stages into which these changes are divided, whether or not the extent of the necrosis is quantitated, which technique is used for quantitation, whether symptomatology and physical findings are included, and which of the various methods of evaluation is employed. When a system is cited, one must also know which specific version of that system is being referred to, because there may be substantial differences between them. The characteristics of the ideal system of staging were outlined earlier. It must be neither too simplistic nor too complex. Although the simple three- and four-part systems are easier to remember and to use, they often do not provide enough information to be effective. For example, the staging system of Ficat and Arlet started with three stages, then went to four, and finally to six; and it has been acknowledged that further classifications to quantitate lesion size should be added. Conversely, if a system becomes too com-

plex, it may confuse rather than assist the user and may not be employed. For example, the ARCO system superimposed on its original version a subset of classifications designed to localize the lesion. This addition made the system so cumbersome and complex that the following year a third version was proposed to simplify it [22,23,25]. It is not practical to have a classification system that includes every feature of the hip being evaluated, and certain important information should be gathered in addition to that used for the classification. For example, it is essential to know the clinical status of a hip in regard to pain and function to determine the optimum treatment. This information should be included in an effective hip evaluation protocol and not incorporated within the classification per se. If one is considering certain specific operative procedures such as rotation or angulation osteotomies, one must know not only the size but also the extent and location of the lesion as it affects the articular surface. The need for this information has been clearly demonstrated by Sugioka as it relates to his rotational osteotomy, but this determination is made as a supplement to his system of classification [11]. The earlier systems for classification did not include any method of quantitation. Even at the present time, the most commonly used classification is that of Ficat and Arlet, which is nonquantitative. Neverthe1ess, almost all workers in this field accept the importance of quantitation and acknowledge that the size and extent of the necrotic lesion does correlate with outcome and must be considered in determining which treatment to use. Quantitation also allows the physician to follow the progression or stabilization of the necrosis more accurately than a nonquantitative system does. Although the need for quantitation has been accepted, differences of opinion remain as to how quantitation can best be done. Lesions can be measured in a variety of ways. One of the simpler methods was described by Kerboul et al [16] in I974 and consists of measuring the ang1e of the necrotic segment as seen on the anteroposterior and the lateral radiographs and simply adding them. This method was later modified and applied to MRI by Koo and Kim [33]. MRI and CT measurements, although perhaps more precise, are costly and complex and generally do not provide much additional information if the lesion is well demarcated on plain radiographs. Plain films are only two-dimensional, however, and lesions of the femoral head occur in three dimensions. Therefore some method must be used to take this third dimension into consideration. In the University of Pennsylvania system, for example, the area of the lesion is measured on both the anteroposterior and

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lateral films using a simple computerized program. These values are then multiplied rather than added, giving a more accurate indication of the volume of the head that is necrotic. The accuracy of this measurement was confirmed by serial MRI measurements [14,15]. In clinical use it is often sufficient simply to estimate rather than measure lesion size. With experience one can achieve close correlation between these estimates and measurements. For example, the authors found that in 54 out of 60 hips the estimate of stage and lesion size was the same as that obtained by actual measurement. In six cases the stage was the same, but the lesion size differed by one grade (ie, A, B, or C). In addition to the size of the necrotic segment, it is important to determine the amount of articular surface affected and the extent of flattening if this is present. One can use marked templates or a simple planimeter to measure the length of the entire articular surface and the length of the segment affected by necrosis, which is then expressed as a percentage of the entire head. The amount of depression is measured by reconstituting the head with concentric circles. Different radiographic projections have been used, and some prefer to average the findings on anteroposterior and lateral films, whereas others have taken measurements only from that view which shows the greatest surface involvement. The authors prefer the latter technique and believe that it gives a more accurate indication of three-dimensional involvement. For example, a small area of flattening or a crescent sign may be seen in only one of two views, and averaging in a negative film would underestimate the true extent of involvement. Regardless of which method is used to determine lesion size, most of these are reasonable estimates rather than precise measurements. Although there is naturally some variation between different techniques, from a practical standpoint the information they provide is similar and is of clinical value. The Japanese Investigation Committee attempted to include a separate category for the location as well as the size of the lesion [20]. This category was subsequently incorporated into the latter two versions of the ARCO classification [23,25]. Many investigators, however, believe that this category adds an unnecessary degree of complexity and provides little useful information. Most lesions are in the anterior superior aspect of the femoral head and extend both medially and laterally as the lesion enlarges. They do not progress from medial to central to lateral as implied (see Fig. 1). This extension was documented by the Japanese investigators themselves, who found

281

that very few lesions were isolated to the medial or medial and central portions of the femoral head [17,18,21]. If it is essential to know which portion of the articular surface is involved (eg, to plan an angulation or rotational osteotomy), the involvement should be measured directly from the lateral view. In the Japanese system only anteroposterior views are considered. Accordingly, the authors believe that so long as a classification includes quantitation of lesion size, it is unnecessary to add a separate category for location. Opinions vary as to the reliability and reproducibility of any of these systems for classification. Some feel that there is considerable inter- and intraobserver variation [45,46]. One of the problems inherent in some of the earlier systems is that they do not always make a clear distinction between different stages. Plakseychuk et al [46] have accordingly suggested abandoning attempts to make relatively subtle distinctions between stages or to quantitate lesion size and have suggested the use of a simple three-part system of staging. Others, however, have found a reasonable degree of reliability and reproducibility and advocate the continued use of comprehensive methods of classification that make a clear distinction between stages and that include quantification [14,15, 17,34] Whichever methods are used, the best results will be achieved if one insists on good-quality anteroposterior and lateral radiographs, on the limited use of CT and MRI when these studies will give information not available on plain films, and on evaluation by experienced examiners. There will always be a certain degree of variation in serial evaluation of radiographs and other imaging studies, but this variation is not so great as to negate the usefulness of these estimates and measurements.

Summary It is hoped that these observations will give the reader a better understanding of the items of fundamental importance in classifying and evaluating osteonecrosis and of the essential features of several major systems in current use. This understanding should make it easier for the reader to compare the results of studies that use different classification systems and to decide which method of classification he or she prefers to use. The authors look forward to that time when workers in the field will agree to the use of a single effective system of classification. Such a system will enable investigators to communicate better with each other, to compare different methods

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of treatment more effectively, and to improve their understanding and management of this most frustrating condition.

[14]

[15]

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