Extract
Articular cartilage injuries (
Fig. 1 ) are common findings during arthroscopy
1 and diagnostic imaging of the joints
2,3 . While there are many techniques for the treatment of cartilage injuries, not enough is known about which lesions need treatment or about the proper treatment modality for a particular lesion. More objective data regarding cartilage injuries and more accurate methods to evaluate the operative outcomes are required, especially since new procedures are becoming increasingly expensive. There are many published reports on the outcomes of total joint replacement based on clinical scores and radiographic evaluations. However, it has been quite difficult to interpret the reported results of the repair of focal cartilage defects as there is no universally accepted system to describe the lesions, the repair tissue, or the clinical symptoms for this category of patients. More studies on clinical articular cartilage resurfacing will appear in the future, making it important to develop common evaluation measurement tools and standards. The International Cartilage Repair Society (ICRS) was founded in 1997 and has been interested in developing a standardization system for the evaluation of cartilage injury and repair
4,5 . A working group of the ICRS was established with the aim of developing a common, easy system for clinical and arthroscopic evaluation (
Table I ). Shortly thereafter, the Articular Cartilage Imaging Committee of the ICRS was created to assess the existing clinical imaging techniques, to recommend specific magnetic resonance imaging techniques for the assessment of articular cartilage
6 , and to develop a standardized magnetic resonance imaging evaluation system for native and repaired cartilage (
Table I ). A state-of-the-art system for clinical cartilage evaluation and imaging assessment is presented below.
Articular cartilage injuries (
Fig. 1 ) are common findings during arthroscopy
1 and diagnostic imaging of the joints
2,3 . While there are many techniques for the treatment of cartilage injuries, not enough is known about which lesions need treatment or about the proper treatment modality for a particular lesion. More objective data regarding cartilage injuries and more accurate methods to evaluate the operative outcomes are required, especially since new procedures are becoming increasingly expensive. There are many published reports on the outcomes of total joint replacement based on clinical scores and radiographic evaluations. However, it has been quite difficult to interpret the reported results of the repair of focal cartilage defects as there is no universally accepted system to describe the lesions, the repair tissue, or the clinical symptoms for this category of patients. More studies on clinical articular cartilage resurfacing will appear in the future, making it important to develop common evaluation measurement tools and standards. The International Cartilage Repair Society (ICRS) was founded in 1997 and has been interested in developing a standardization system for the evaluation of cartilage injury and repair
4,5 . A working group of the ICRS was established with the aim of developing a common, easy system for clinical and arthroscopic evaluation (
Table I ). Shortly thereafter, the Articular Cartilage Imaging Committee of the ICRS was created to assess the existing clinical imaging techniques, to recommend specific magnetic resonance imaging techniques for the assessment of articular cartilage
6 , and to develop a standardized magnetic resonance imaging evaluation system for native and repaired cartilage (
Table I ). A state-of-the-art system for clinical cartilage evaluation and imaging assessment is presented below.
The best known arthroscopic cartilage lesion classification system was developed by Outerbridge
7 . This system divides lesions into four grades (grades I through IV) and is easy to understand and to use. However, Outerbridge grades II and III do not include a description of the lesion depth. Other arthroscopic classification systems include other variables such as articular surface appearance, lesion depth, lesion diameter, and location
8,9 . However, those systems have not been widely used or are more appropriate for the evaluation of osteoarthritis than for the classification of focal cartilage lesions
9 . Most physicians who use those systems agree that there is a need for a more precise description of the location, depth, and size of the lesion along with a description of the surface and quality of the surrounding cartilage. Furthermore, it seems important to have a simpler classification system that provides a descriptive and, if possible, a prognostic analysis of the injured cartilage to simplify the decisions of treatment planning.
Magnetic resonance imaging has emerged as a promising noninvasive method for the assessment of articular cartilage abnormalities. While the initial results associated with the use of standard spin-echo pulse sequences for the detection of articular cartilage lesions were disappointing, newer magnetic resonance imaging techniques have proven to have sensitivities of >95% for the detection of focal abnormalities
2,3,10-14 . As with all medical imaging techniques, lesion detection is dependent on the image contrast between abnormal and normal tissues, the signal-to-noise ratio of the image, and the spatial resolution of the imaging technique. Fast-spin-echo (with or without fat suppression) and/or fat-suppressed (or water-selective excitation) spoiled gradient-echo image acquisitions are strongly recommended
6 .
To achieve the sensitivities and specificities for articular cartilage lesion detection that have been reported in the literature, the pulse sequences must be combined with high spatial resolution acquisition parameters since the tissue is thin, usually <4 mm, and the articular surfaces are curved, leading to "partial volume" artifacts. When an image voxel contains two different tissues of differing signal intensities, the signal intensity of the voxel that appears in the final image is an average of the two signal intensities, weighted by the proportion of each tissue within the voxel. With high-field magnet systems (=1 T), typical voxel dimensions used for high-resolution clinical imaging of the knee are 0.3 to 0.5 mm in plane with a slice thickness of between 3 and 4 mm (field of view, 14 cm; matrix, 512 × 256). These dimensions limit the accuracy of measurement of articular cartilage thickness, the depth or size of a defect, or the presence of a fissure. The magnetic resonance imaging techniques recommended by the Articular Cartilage Imaging Committee of the ICRS can be found in
Table II .
Transarthroscopic Assessment
During the arthroscopic assessment of cartilage lesions, partially detached fragments need to be excised and removed since firm, regular edges make the defect stable. The depth of the lesion is analyzed with use of a graduated hook. Each fissure is followed carefully in order to detect any crevice that extends to the bone, thereby revealing that an apparently shallow defect is actually a deep, potentially troublesome defect (
Figs. 2-A and
2-B ). A nerve probe with a lengthened arm with marked units of measurement could be used to measure the dimensions of the débrided defect assuming that the defect is more or less rectangular in shape to record the length (a mm) and width (ß mm). In a recent study, Oakley et al.
15 reported a variation in accuracy and poor interobserver reliability of cartilage lesion measurement with use of conventional methods and found that the accuracy of measurement could be improved with special variable-angle elongated probes.
Imaging Assessment
To date, no standardized magnetic resonance imaging classification system for articular cartilage lesions has been accepted. However, most grading methods have used a variation of the Outerbridge arthroscopic classification system to record lesion depth. Many studies have shown that Outerbridge grade-1 lesions (softening) are not reliably detected with magnetic resonance imaging
11-13 . At a minimum, superficial fissuring, fibrillation, or shallow ulceration must be present before a lesion is detectable. Several studies have shown variable correlations between Outerbridge grades assigned on the basis of magnetic resonance imaging and those assigned on the basis of arthroscopy. In those studies, the rate of precise agreement ranged from 47% to 96% whereas the rate of agreement within one grade ranged from 90% to 100%
3,10,11,14 .
To our knowledge, no study has directly evaluated the accuracy of magnetic resonance imaging in measuring the dimensions of articular cartilage defects. However, it is clear from our clinical experience that determination of the size and depth of a cartilage lesion with use of magnetic resonance imaging can be challenging and is dependent on the status of the lesion. Extrapolating from theoretical modeling of the accuracy of magnetic resonance imaging for the measurement of cartilage thickness, if a cartilage lesion is an "empty" defect with sharply defined margins and without partially attached fragments or unstable margins, magnetic resonance imaging should be able to assess the size and depth of the lesion with a maximum error of the dimension of one voxel and a minimum error of 40% of one voxel, depending on the image acquisition technique
16 . However, magnetic resonance imaging most often is performed prior to the débridement of the cartilage defect, which contains partially attached fragments, thereby leading to an underestimation of the length and width of the lesion (
Figs. 3-A and
3-B ). Similarly, since the depth of a lesion is determined arthroscopically by the deepest extent of a probe, a very thin but deep fissure can be easily lost within partial-volume artifacts on magnetic resonance images, leading to an underestimation of the depth of the lesion. Magnetic resonance imaging, however, has an advantage over arthroscopy in determining the osseous extent of the lesion since it directly images the subchondral bone and bone marrow.
The débrided, stabilized lesion should first be defined as a superficial, partial-thickness, or full-thickness cartilage defect. The ICRS classification system focuses on the lesion depth (graded from 0 to 4) and the area of damage (graded from normal to severely abnormal with use of the IKDC system
17 ) (
Fig. 4 ).
Macroscopically normal cartilage without notable defects is classified as ICRS 0 (normal). If the cartilage has an intact surface but fibrillation and/or slight softening is present, it is classified as ICRS 1a, and, if additional superficial lacerations and fissures are found, it is classified as ICRS 1b (nearly normal). Defects that extend deeper but involve <50% of the cartilage thickness are classified as ICRS 2 (abnormal). These lesions are often unstable, with partly detached fragments that need to be débrided to form stable lesions. The prognosis for ICRS-2 partial-thickness lesions seems good
18 , with diminished mechanical symptoms following a simple débridement that involves excision of the unstable cartilage fragments back to smooth edges and leaves the base intact. In the literature, the deep to bare-bone lesions seem troublesome
19 . Lesions that extend through >50% of the cartilage thickness are classified as ICRS 3 (severely abnormal). There are four subgroups of this grade: deep defects that extend through >50% of the cartilage depth but not to the calcified layer are classified as ICRS 3a, deep defects that extend through >50% of the cartilage depth to the calcified layer are classified as ICRS 3b, defects that extend down to but not through the subchondral bone plate are classified as ICRS 3c, and, finally, blisters are classified as ICRS 3d. All of the lesions in category ICRS 3 are simply defined as defects that extend through >50% of the cartilage thickness, through the cartilage but not through the subchondral bone plate. While débridement of unstable edges (as is suggested for ICRS-2 lesions) is suitable for ICRS-3 lesions, further treatment is recommended for these more extensive lesions. A simple treatment is to imitate the vascular tissue inflammatory phase by opening the subchondral space with use of drilling, intracortical abrasion, or microfracture techniques. A combination of drilling and perichondral or periosteal grafting is possible. Allografting or autografting with osteochondral grafts is another treatment option, as is the use of autologous grafted cultured chondrocytes.
Joint trauma may create cartilage defects that extend into the subchondral bone. These full-thickness osteochondral injuries are classified as ICRS 4 (severely abnormal). Excluded from this grade are defects that are classified as osteochondritis dissecans (OCD), which have a classification system of their own (discussed below). ICRS-4 lesions can be treated in the same manner as described for ICRS-3 lesions, but a lesion with extensive cavitation into the bone may require bone-grafting.
Osteochondritis dissecans is an osteochondral disease that can be diagnosed with radiographs, which can be used to determine the extent of osseous involvement and the depth of the lesion. However, an arthroscopic description of the osteochondral fragmentation is needed, and the ICRS has suggested the following classification system (
Fig. 5 ). Stable lesions with a continuous but softened area covered by intact cartilage are classified as ICRS OCD I, lesions with partial discontinuity that are stable when probed are classified as ICRS OCD II, lesions with a complete discontinuity that are not yet dislocated ("dead in situ") are classified as ICRS OCD III, and empty defects as well as defects with a dislocated fragment or a loose fragment within the bed are classified as ICRS OCD IV. Subgroups ICRS OCD I-IVB are defects that are >10 mm in depth.
More active research is needed in order to correlate magnetic resonance imaging findings with the ICRS cartilage lesion classification. However, the available clinical and research data allow some preliminary observations. As in most magnetic resonance imaging studies with the clinically used acquisition techniques, very little morphologic alteration in ICRS-1a lesions have been reported and therefore it is difficult to differentiate these lesions from normal (ICRS-0) cartilage. In one study
14 involving fat-suppressed fast-spin-echo imaging, areas of softening were detectable as regions of cartilage signal abnormality without detectable morphologic changes. dGEMRIC, a magnetic resonance imaging technique that is beginning to be used in clinical studies, is sensitive to the concentration of glycosaminoglycan within the cartilage matrix and shows great promise for the detection of cartilage softening and superficial fibrillation (i.e., ICRS-1a lesions)
20 . Since ICRS-1b lesions (superficial lacerations and fissures) are deeper, they should be more easily detected with magnetic resonance imaging. However, the differentiation of ICRS-1b lesions from ICRS-1a and ICRS-2 lesions may be difficult.
The spatial resolution of magnetic resonance images is usually adequate to determine whether a cartilage defect involves >50% of the cartilage thickness (ICRS 3) or <50% of the cartilage thickness (ICRS 2). However, if the deepest part of the lesion is very focal and narrow, the grade of the lesion may be underestimated with magnetic resonance imaging. The deepest layers of articular cartilage usually appear dark on magnetic resonance images, similar to the appearance of the subchondral bone plate. Therefore, at this time, it is unlikely that magnetic resonance imaging will be able to differentiate among ICRS-3a lesions (which do not extend into the calcified cartilage layer), ICRS-3b lesions (which extend down to the calcified layer), and ICRS-3c lesions (which extend down to but not through the subchondral bone plate). Blistering (ICRS-3d lesions) may be detected as a bulge on the cartilage surface.
Magnetic resonance imaging can be used to directly visualize the subchondral bone and bone marrow. Changes in the signal intensity of the subchondral bone marrow can be an indirect sign that there is an overlying cartilage lesion
21 . ICRS-4 cartilage lesions, which extend into the subchondral bone, are often detected by the presence of a subchondral cyst beneath them. Even if the direct communication between the cartilage defect and the cyst cannot be identified on the images, direct communication should be strongly suspected. Similarly, except in the setting of acute trauma when a bone bruise may be present, if there is a focal edema-like signal in the marrow beneath a cartilage lesion, it may indicate that the lesion extends to, or into, the subchondral bone plate (suggesting a classification of ICRS 3 or ICRS 4). As with the arthroscopic grading of lesions, the grading of the depth of a lesion found with magnetic resonance imaging should be recorded as the greatest depth observed within the lesion.
In general, magnetic resonance imaging will tend to underestimate the true size of the dimensions of a cartilage defect. Since most cartilage defects have irregular, ovoid shapes, it is unlikely that any one magnetic resonance image will be perfectly aligned to demonstrate the maximal length or width of a lesion. Therefore, measurement of the distance between the margins of a defect may extend over several image slice locations and will increase the difficulty of obtaining an accurate assessment of lesion size. Magnetic resonance imaging may also underestimate the dimensions of a lesion when unstable fragments remain in place along the margins of a defect.
Magnetic resonance imaging has proved useful for determining the extent and stability of OCD lesions
22-25 . De Smet et al.
23 showed that the presence of any one of four magnetic resonance imaging findings indicates an unstable OCD lesion. These findings include (1) a line of high signal deep to the fragment as seen on T2-weighted images, (2) an articular fracture indicated by high signal passing through the subchondral bone plate, (3) a focal osteochondral defect, and (4) a 5-mm-diameter fluid-filled cyst deep to the lesion
23 . Other authors have suggested that the presence of a bright line deep to the OCD fragment may result from granulation tissue and that a break in the articular surface must be demonstrated with magnetic resonance imaging to be sure that the fragment is unstable
22,24 (
Figs. 6-A and 6-B ). Intra-articular magnetic resonance arthrography appears to improve the identification of unstable fragments
26 . Therefore, on magnetic resonance images, ICRS OCD-I lesions should not demonstrate any of the four criteria described by De Smet et al.
23 . Without a directed study, it is uncertain whether magnetic resonance imaging can differentiate ICRS OCD-II from ICRS OCD-III lesions. Magnetic resonance imaging can detect displacement of the fragment from the bed, which should allow proper staging of ICRS OCD-IV lesions.
Dividing the knee joint into sectors makes it easier to describe lesion location, and a simplified mapping system has been agreed upon (
Fig. 7 ). The lesion location needs to be described precisely and to be mapped on both the frontal and the lateral view. The utility of such a mapping system has been discussed, and further validation may be needed
27 . If the total joint involvement can be assessed with percentages and/or with such a scoring system, perhaps with the aid of a computer-based system, the progression or improvement of cartilage disease can be followed.
Cartilage repair should be evaluated with use of a system that considers the volume of the defect that becomes filled with repair tissue, the integration of repair tissue with adjacent articular cartilage, and the macroscopic appearance and biomechanical properties of the repair site (
Table III ). The various repair methods have different starting points. Some will progressively fill the defect with tissue while others will immediately fill the defect. These repair features must be taken into consideration early in the postoperative period.
Tissue repair is assessed on the basis of three criteria: the degree to which the defect is filled with repair tissue, the integration of repair tissue with adjacent articular cartilage, and the macroscopic surface appearance. Each part of this subjective arthroscopic evaluation is assigned a maximum score of 4 points. The repair is then classified as grade I (12 points), grade II (8 to 11 points), grade III (4 to 7 points), or grade IV (0 to 3 points).
Magnetic resonance imaging can be used to noninvasively examine both the degree to which the defect is filled with repair tissue and the integration of repair tissue with adjacent tissues
28-30 . Additionally, magnetic resonance imaging can be used to evaluate the subchondral bone plate and marrow beneath the repair site
29,30 . The methods that have been proposed for the assessment of cartilage repair with use of magnetic resonance imaging are similar in that they evaluate each feature of the repair rather than provide an overall score for the repair
28 . One goal of the Imaging Committee of the ICRS is to standardize the method used to evaluate magnetic resonance imaging studies of cartilage repair. Some variation in the repair assessment system will be required to accommodate different operative techniques. The components of an evaluation method that incorporates most of the elements thus proposed are provided below as a starting point for a magnetic resonance imaging assessment system for cartilage repair.
The fill of a cartilage defect usually requires a judgment to be made on the basis of several magnetic resonance images and may be recorded as the percentage of the volume of the defect that is filled by repair tissue
28 . An estimate of the minimum and maximum thickness of the repair tissue as a percentage of the thickness of adjacent native cartilage should also be recorded. When hypertrophic repair tissue is present, the maximum thickness will be >100% of the native cartilage thickness. If an osseous defect was part of the original lesion, this should be excluded from the thickness measurement and a separate estimation of the fill of the bone defect should be made (
Fig. 8 ). When possible, the amount of osseous and soft-tissue fill should be differentiated in the documentation.
Integration of the cartilage repair tissue with adjacent tissues must be determined on the basis of an assessment of the integration with adjacent articular cartilage as well as with subchondral bone, or, in the case of osteochondral defects, incorporation of the osseous portion of the graft into the bone. On magnetic resonance images, the interface between well-incorporated repair tissue and adjacent articular cartilage may appear as a sharp interface between tissues of different signal intensities, as a dark line, or may be indiscernible. An interface that consists of fluid-like signal intensity suggests that integration between the repair tissue and the native cartilage is incomplete and that a fissure may exist. However, in the case of autologous chondrocyte implantation (ACI), a bright interface may be visible even if a surface fissure is not demonstrable with arthroscopy
31 . This finding suggests that either the integrating repair tissue has fluid-like signal or that the bright interface represents incomplete integration of the repair beneath an intact periosteal cover that is not detected with magnetic resonance imaging. The formation of subchondral cysts beneath the interface indicates failure of integration of the repair tissue-cartilage interface (
Figs. 9-A and 9-B ).
Failure of the repair tissue to integrate with the underlying subchondral bone may result in delamination of all, or a portion, of the repair tissue from the subchondral bone. The delaminated repair tissue may be displaced or remain in situ. On magnetic resonance images, a displaced delamination appears as a cartilage defect at the repair site. Often, the displaced repair tissue can be found elsewhere in the joint
31 . An in situ delamination of the repair tissue has an appearance similar to a flap tear of articular cartilage with fluid-like signal or, following arthrography, with contrast medium extending beneath the repair tissue, between the repair tissue and the subchondral bone plate. A visible communication between the joint space and the fluid beneath the delaminated portion of the repair is commonly identified. The location and size (as a percentage of the total area of the repair) should be reported along with the size and presence of any associated subchondral cysts.
In the early postoperative period, edema-like signal in the marrow subjacent to a cartilage repair site is a common finding with all methods of repair
29,30 . As the repair site heals, the edema-like signal regresses, although the precise timeline for the normalization of the marrow signal is unknown. For osteochondral grafts, the edema-like signal appears to resolve as incorporation of the graft bone into the recipient progresses. However, as with other cartilage repair techniques, persistence or intensification of the abnormal marrow signal may indicate a failure of graft incorporation.
The intensity and extent or depth of the abnormal edema-like marrow signal should also be reported. A proposed system for grading the extent of marrow signal abnormality within the knee (femur and tibia) is shown in
Figure 10 . Abnormal signal is graded as superficial (beneath the subchondral plate), shallow (extending as far as one-third of the distance from the articular surface to the physeal scar), deep (extending between one-third and two-thirds of the distance to the physeal scar), extensive (extending at least two-thirds of the distance to the physeal scar but not beyond the scar) or generalized (extending beyond the physeal scar). The intensity of the signal on fat-suppressed magnetic resonance images (proton density-weighted, T2-weighted, short tau inversion recovery [STIR], or contrast-enhanced T1-weighted images) is classified as mild when less than that of muscle, as moderate when equal to that of muscle, or as intense when brighter than that of muscle.
Even if both magnetic resonance imaging and macroscopic arthroscopic views show a nicely grafted area, the patient still may not be satisfied with the clinical result. How should the clinical outcome of a cartilage articular resurfacing be evaluated, and when is it appropriate to perform such an evaluation?
Regardless of the type of cartilage injury, the presence of focal defects, or the presence of widespread osteoarthritis, assessing the clinical response to cartilage repair methods requires the use of a validated, reliable, and responsive measurement technique. The clinical evaluation should be reproducible and have high reliability and high sensitivity. A comprehensive evaluation of the operative results should consist of a self-administered patient questionnaire that measures outcome after knee trauma as well as a clinical examination technique combined with an easy, usable description of the kind of lesions that have been treated. The assessment should clearly differentiate between a local, well-contained cartilage defect and an osteoarthritic lesion, which is part of a more generalized joint process. The ICRS endorses two clinical evaluation forms: the newly revised IKDC form
17 (http://www.sportsmed.org/pdf/IKDC.pdf) and the recently developed and validated KOOS (Knee Osteoarthritis and Injury Outcome Score) (www.koos.nu)
32 . Both systems can be used separately or in comparison. Health-related quality-of-life measures are considered to be increasingly important components of long-term studies. The IKDC contains a variant of the SF-36 instrument, and the KOOS also has a section referring to health-related quality-of-life measures. The ICRS Evaluation Package collects both symptomatology data and lesion description, including mapping and repair assessment. The ICRS Evaluation Package may be downloaded without cost from www.cartilage.org
33 .
Together with a group at Stanford University, ICRS is also developing an Internet-based computer database. This database incorporates a three-dimensional model of the knee for the collection of cartilage lesion data, which may facilitate future multicenter studies. The data on a number of different cartilage lesions in one knee could then be input into a computer program for an exact calculation of lesion volume, overall severity score, and clinical outcome. In addition, the data could then be cross-correlated and eventually pooled.
In 1993 Bellamy
34 wrote that "despite more than fifty years experience with outcome measurement in musculoskeletal clinical trials, there remains a diversity of opinion and a lack of adequate standardization in the methods employed" Therefore, in the new millennium, it is hoped that basic and clinical researchers can unite to develop and use standardized systems for the evaluation of cartilage lesions, cartilage repair tissue, and clinical outcomes of cartilage resurfacing methods. Articular cartilage is a tissue that undergoes continuous remodeling during its lifetime, and a common evaluation system for the assessment of cartilage and cartilage repair will likewise require continuous remodeling to become as perfect as possible.
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