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The knee: bone marrow abnormalities
Radiol Clin N Am 40 (2002) 1109 – 1120
The knee: bone marrow abnormalities Michelle S. Barr, MD*, Mark W. Anderson, MD Department of Radiology, University of Virginia Health System, Charlottesville, VA 22908, USA
MRI is an invaluable tool for assessing the bone marrow. It is the most sensitive imaging modality for detecting marrow pathology and simultaneously provides a detailed depiction of the adjacent soft tissues. This article describes the appearance of normal and abnormal bone marrow in and around the knee as depicted with MRI.
Normal bone marrow Bone marrow is categorized into two types of tissue based on differences in their color at gross pathologic examination. The active, hematopoietic component is comprised mostly of erythrocytes and their precursors and is denoted as ‘‘red’’ marrow, whereas ‘‘yellow’’ (inactive) marrow is comprised primarily of fat. Each type of marrow displays a distinctive appearance on MRI based on the relative amounts of fat and water within it. Because fat tends toward very short T1 and moderately long T2 relaxation times, yellow marrow exhibits high signal intensity on T1-weighted and fast spin echo T2-weighted images, intermediate signal intensity on conventional T2-weighted images, and variable signal intensity on gradient echo images depending on the amount of trabecular bone present. On fat-saturated sequences, yellow marrow demonstrates relatively homogeneous signal intensity that is lower than that of muscle. Contrast administration results in only minimal alteration in the yellow marrow signal intensity [1]. The signal characteristics of red marrow stem from its higher percentage of water (40% versus 15% in
* Corresponding author. E-mail address: [email protected] (M.S. Barr).
yellow marrow). On T1-weighted spin echo and fast spin echo imaging, it exhibits lower signal intensity than fat, whereas demonstrating higher signal intensity than that of muscle. Red marrow demonstrates intermediate to high signal intensity on short tau inversion recovery (STIR) or fat-suppressed T2weighted images and variable signal characteristics on gradient echo images (Fig. 1). Enhancement of red marrow is minimal in adults but can be quite marked in children [1].
Normal marrow conversion The normal distribution of red and yellow marrow varies with age. In utero and through childhood, hematopoietic marrow predominates. Shortly before birth, marrow in the distal phalanges converts from red to yellow. This process normally progresses with age from distal to proximal within the appendicular skeleton. Not only does bone marrow conversion progress from the most distal to the most proximal portions of the skeleton, but it also progresses in a predictable fashion within each bone. Within a long bone, the conversion from red to yellow marrow starts in the diaphysis, in the region of the central diaphyseal vessels, and extends both proximally and distally toward each end. The epiphysis is different because it converts to fatty marrow early in infancy when it begins to ossify. Low signal intensity marrow within an epiphysis on T1-weighted images is abnormal if it is seen later than 6 months after the ossification center first appeared [1]. Yellow marrow occupies most of the diaphysis in a child’s long bone during the first decade of life, and is identified on T1-weighted images by its relatively bright fat. Conversion from red to yellow marrow
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Fig. 1. (A) Normal marrow. Coronal T1-weighted image shows a normal adult marrow pattern. Note the metadiaphyseal hematopoietic marrow, which is slightly hyperintense to muscle and sharply marginated at the old physeal plate (arrow). (B) Coronal short tau inversion recovery image highlights the hyperintense hematopoietic marrow adjacent to the dark, saturated fat of the yellow marrow elsewhere in the bones.
continues to occur throughout the second decade, although some residual red marrow is retained in the proximal humeral and femoral metaphyses. The adult marrow pattern is present by 25 years of age. At this point, red marrow is found predominantly in the axial skeleton, sternum, ribs, and proximal metaphyses of the femora and humeri (Fig. 2). Marrow conversion slows at this point and becomes
dependent on variables, such as gender, nutritional status, obesity, activity, medications, smoking, and age [1 – 3]. Reconversion of yellow to red marrow occurs in areas where sinusoidal networks and perivascular reticular cells can appear rapidly: metaphyseal and metaphyseal equivalent regions, subchondral epiphyseal areas, and diaphyseal endosteal spaces. This
Fig. 2. Adult marrow pattern. Coronal T1-weighted MRI of the pelvis demonstrates red marrow within the pelvis and proximal femurs with fatty marrow in the femoral heads and greater trochanters.
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pattern is the reverse of red to yellow conversion in that reconversion to red marrow begins in the ends of the bones and progresses toward the mid-diaphyses. Difficulties may arise when attempting to distinguish normal red marrow from marrow pathology. There are several imaging features that favor the diagnosis of hematopoietic marrow. Most types of marrow pathology result in signal intensity that is lower than that of skeletal muscle or intervertebral disk on T1-weighted images, whereas hematopoietic marrow demonstrates signal intensity that is slightly higher than that of skeletal muscle or disk on T1weighted images (owing to the relatively high amount of fat present even in red marrow). Other features of red marrow include signal intensity that parallels the signal intensity of other areas of known hematopoietic marrow, bilateral symmetry, scattered foci of fatty signal within the region of concern, and an abrupt margination at the level of a closed physis (see Fig. 1) [1,2]. In some adults, however, red marrow also may extend into the epiphyseal regions. Although normalappearing bone marrow on MRI does not definitively exclude the possibility of disease, a thorough understanding of the MRI appearance of normal hematopoietic marrow allows for an improved ability to distinguish the normal from the pathologic.
Marrow pathology
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pattern within the marrow that is most conspicuous on fat-saturated T2 or STIR images (Fig. 3). Direct trauma to the bone can produce a focal contusion, but these most often result from one bone impacting on another. The ‘‘kissing contusions’’ often seen with anterior cruciate ligament tears are a classic example of this type of injury (Fig. 4). Evaluation of a contusion pattern often reveals the mechanism of injury and predicts associated soft tissue pathology. The marrow abnormalities may also prompt a careful search for less easily detected avulsive injuries that may result in joint instability necessitating surgical intervention [5,6]. Acute avulsive injuries Distraction injuries usually occur in response to rotational, varus, or valgus stress on a joint and often result in a small avulsion fracture related to a tendinous, ligamentous, or capsular attachment on the bone. The associated marrow edema is much less extensive than the edema seen with an impaction injury because cortical rather than medullary bone is involved [4 – 7]. The avulsed fragment can be very difficult to detect by MRI because there is usually a disproportionate amount of edema and hemorrhage in the adjacent soft tissue that may mask the small osseous fragment. A small avulsion fragment is often demonstrated better on conventional radiographs (Fig. 5).
Entities that affect the bone marrow are varied and include trauma, osteonecrosis, infection, tumors, arthritides, and metabolic disorders. Bone marrow typically demonstrates a similar response, however, regardless of the insult: increased fluid content in the form of edema, hemorrhage, pus, or tumor [3,4]. With this limited repertoire, it seems nearly hopeless that MRI could provide any specificity when attempting to differentiate between these varied etiologies, but a systematic approach of analyzing the pattern of marrow pathology and associated abnormalities often helps to limit the differential, or even arrive at a specific diagnosis.
Trauma Acute impaction injuries An acute impaction force on a bone results in marrow hemorrhage and edema, disruption of trabeculae, and interstitial fluid leakage within the marrow space. On MRI, these bone bruises (contusions) are identified by the vague, geographic, edema-like
Fig. 3. Bone contusion. Coronal short tau inversion recovery image demonstrates vague geographic edema in the lateral tibial condyle compatible with a bone marrow contusion.
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that is exacerbated with activity and relieved with rest. Palpation often reveals tenderness and soft tissue swelling over the site of osseous damage [8,9]. MRIs reveal a spectrum of findings from periosteal edema alone, to progressively severe marrow edema, to a hypointense fracture line in cancellous or cortical bone (Fig. 6). The fracture line is most often of a transverse or oblique orientation within a long bone, but longitudinal stress fractures also have been described [10]. Chronic avulsive injuries
Fig. 4. Anterior cruciate ligament tear contusion pattern. Sagittal T2-weighted fat-saturated MRI demonstrates the ‘‘kissing contusion’’ pattern often seen with anterior cruciate ligament tears. Subchondral edema-like signal is present in the lateral femoral condyle and the posterolateral tibial plateau.
Fatigue and insufficiency fractures Fatigue and insufficiency fractures demonstrate similar radiographic and MRI findings. Fatigue fractures develop when abnormal stress is applied to normally mineralized bone, whereas insufficiency fractures result from normal activities applied to weakened bone. Clinically, these injuries induce pain
‘‘Shin splints’’ refers to a syndrome of activityrelated lower leg pain that has long been thought to be related to a traction periostitis of the calf muscle along the posteromedial tibia. In addition to the expected periosteal edema or fluid, MRI has also revealed marrow edema and even cortical signal abnormalities that indicate osseous stress injuries of varying degrees [8,11]. Thigh splints (adductor insertion avulsion syndrome) is a similar condition and refers to activityrelated groin or thigh pain that is thought to be related to the pull of the adductor tendons on the proximal to mid femoral shaft. As with shin splints, MRI reveals a spectrum of osseous injury from periosteal edema or fluid to varying degrees of marrow edema (Fig. 7) [12]. The avulsive cortical irregularity syndrome (cortical desmoid) occurs along the posterior margin of the distal femur and in some cases can be difficult to distinguish from a paraosteal osteosarcoma. The MRI appearance may also be confusing. Posch and Puckett
Fig. 5. (A) Avulsion fracture. Coronal short tau inversion recovery image of the knee reveals a small cortical avulsion fracture (Segond fracture) along the lateral tibial plateau (black arrow). Compare the prominence of the soft tissue edema with the paucity of marrow edema (white arrow). (B) Anteroposterior radiograph of the knee. The fracture fragment is seen more easily.
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Fig. 6. Stress fracture. Coronal short tau inversion recovery image of the proximal lower legs in a child with left lower leg pain reveals a hypointense fracture line extending horizontally through an area of extensive marrow edema in the proximal left tibia. Note also the marked periosteal thickening and soft tissue edema in that region.
[13] describe the features that favor a benign entity: bilateral symmetry (even if the contralateral side is asymptomatic); edema with enhancement at the base of the irregularity, which remains outside of the medullary canal and along the outer confines of the cortex; clinical history of a physically active young child; and minimal uptake on nuclear medicine bone scan. The location of the lesion is characteristic, lying at the medial ridge of the linea aspera just superior to the adductor tubercle (Fig. 8). This site suggests a relationship to the insertion of the adductor magnus
tendon or the origin of the medial head of the gastrocnemius muscle. Spontaneous osteonecrosis As its name implies, spontaneous osteonecrosis is a condition that affects the knee and results in an area of subchondral necrosis. Although long thought to represent a form of primary osteonecrosis, recent studies have concluded that this lesion is actually a subchondral insufficiency fracture that results in a
Fig. 7. Thigh splints. Coronal short tau inversion recovery image of the proximal thighs in this young track runner demonstrates foci of marrow edema along the medial endosteum of the proximal femoral shafts. The changes are slightly worse in the right femur, which also displays mild periostitis (arrow).
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different location in the medial femoral condyle (weight-bearing surface), and a unique MRI appearance. Radiographs are often normal, even though the pain is severe, and the patient is unable to ambulate. On MRI, extensive edema-like signal is seen in the medial femoral condyle along with a linear subchondral focus of low signal intensity that represents the insufficiency fracture (Fig. 9).
Osteonecrosis Medullary infarction
Fig. 8. Cortical irregularity of the distal femur. Sagittal gradient echo T2*-weighted image of the knee shows a welldefined, rounded, intracortical lesion along the posterior metaphysis of the distal femur. Note the edema along the surface of the bone and within the adjacent soft tissues.
devitalized segment of bone between the fracture line and overlying articular cartilage [14]. This most likely explains why this entity can usually be differentiated from osteochondritis dissecans (described later). Spontaneous osteonecrosis typically has an older age of onset (most commonly a middle-aged woman), an abrupt onset of symptoms, a
Several factors are known to predispose to the development of focal areas of medullary infarction. These include the use of exogenous corticosteroids; increased production of endogenous steroids (eg, Cushing’s syndrome); alcohol abuse; pancreatitis; vasculitis; trauma; radiation; hemodialysis; and hemoglobinopathies (sickle cell anemia, thalassemia, polycythemia). Some cases are idiopathic [4,14]. Medullary infarcts result in geographic areas of ischemic and devitalized marrow that produce a characteristic MRI appearance: a geographic focus of typically heterogeneous signal within the marrow that is surrounded by characteristic low signal intensity, serpentine border on T1-weighted images. This border often demonstrates a classic double-line sign on
Fig. 9. (A) Spontaneous osteonecrosis. Coronal short tau inversion recovery (STIR) image of the knee demonstrates extensive edema within the medial femoral condyle extending to the intercondylar notch. (B) Sagittal STIR image of the knee reveals a linear subchondral fracture within the marrow edema (arrow).
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Fig. 10. (A) Medullary infarcts. Sagittal T1-weighted image of the knee demonstrates the classic undulating serpentine border of medullary infarct in the proximal tibia that is pathognomonic for osteonecrosis. Note the central fat, characteristics for this lesion. (B) Sagittal T1-weighted MRI of the knee reveals a second infarct in this same patient in a more subchondral location of the medial femoral condyle.
T2-weighted images that manifests as an inner margin of high signal intensity surrounded by an outer rim of low signal intensity [15,16]. This is one of the few medullary lesions that usually contain some central fat (Fig. 10). In the early stages of an acute medullary infarct, only marrow edema may be present, making it difficult to differentiate this from other types of pathology. Similarly, ischemic foci may present as areas of edema-like signal within the marrow, but unlike a true medullary infarct, these tend to be transitory. Osteochondritis dissecans A special form of subchondral osteonecrosis is termed osteochondritis dissecans. This entity is most frequently seen in adolescents and young adults and refers to fragmentation, and often separation, of a portion of subchondral bone, typically along the lateral aspect of the medial femoral condyle. The cause of this lesion is uncertain but it is thought to result from repetitive trauma that produces shear forces across the cartilage. Radiographic findings include a geographic, subchondral lucency along the non – weight-bearing surface of the medial femoral condyle [17].
MRI plays an important role in detecting the lesion if plain films are normal. A crescentic or ovoid focus of subchondral signal abnormality is evident (Fig. 11). The primary concern when evaluating a focus of osteochondritis dissecans is whether the fragment of subchondral bone is unstable (ie, at risk of evolving into a displaced loose body in the joint), in which case it likely requires operative intervention. Several MRI features have been shown to be suggestive of an unstable fragment. These include fluid tracking between the fragment and host bone, cystic foci at that same interface, or a 5-mm or larger defect in the overlying cartilage. MR arthrography can be used in this setting to confirm that a fragment is truly unstable by demonstrating intra-articular gadolinium tracking between the fragment and host bone (Fig. 12). Transient bone marrow edema syndrome (transient osteoporosis) Transient bone marrow edema syndrome (also known as transient osteoporosis) was first described in the hip. Originally reported in women during their third trimester of pregnancy, this entity also has been
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Fig. 11. Osteochondritis dissecans. Coronal short tau inversion recovery image of the knee. An osseous fragment has partially detached from the lateral non – weight-bearing aspect of the medial femoral condyle (arrowhead ). Cystic changes and some joint fluid are present between the osseous fragment and femoral condyle.
shown to be common in men. Its exact cause is uncertain but several authors have postulated that local trauma, reflex sympathetic dystrophy, bone marrow edema, and insufficiency fractures may actually represent successive stages of a process that could ultimately culminate in osteonecrosis [18].
Affected patients present with an acute onset of pain, usually not associated with trauma. Within 2 to 4 weeks of the initial symptoms, radiographs may reveal femoral head and neck osteopenia with marked indistinctness of the subchondral cortical bone [19]. MRI findings include diffuse, nonfocal, edema (low signal on T1-weighted images and high signal on T2-weighted or STIR sequences) [19,20]. In the knee, the lateral femoral condyle is usually involved, although involvement of the medial femoral condyle and tibial plateau has also been described [15,21]. Resolution of pain and edema usually takes place within 6 to 12 months. Long-term sequelae do not occur. The ability to distinguish transient bone marrow edema syndrome from other entities is difficult and is often a diagnosis of exclusion, with osteonecrosis, reflex sympathetic dystrophy, insufficiency fractures, or trauma constituting other differential possibilities. Reflex sympathetic dystrophy The exact cause of reflex sympathetic dystrophy is unclear but it is believed to represent sequelae from hyperactivity of the sympathetic nervous system. The most common of the varied entities producing this syndrome are trauma, hemiplegia, and myocardial infarction. Reflex sympathetic dystrophy most often affects the upper extremities, and in many cases occurs after
Fig. 12. Osteochondral lesion. MR arthrogram. Coronal fat-saturated T1-weighted MR arthrogram reveals an unstable fragment with gadolinium tracking between the fragment and host bone.
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Fig. 13. (A) Osteomyelitis. Radiograph of the left femur reveals a focal ill-defined lytic lesion in the lateral metaphysis of the digital femur and an aggressive, interrupted periostitis. This proved to represent bacterial osteomyelitis on biopsy. (B) Coronal T1-weighted MRI of the femur reveals disruption of the cortex in the lateral metaphysis of the distal left femur with effacement of the normal fat signal adjacent to the bone (arrow). (C) Coronal short tau inversion recovery image of the femur better demonstrates associated signal abnormality in the marrow and edema involving the soft tissues.
a recent episode of trauma. It results in circulatory changes and may progress to muscle atrophy, contractures, pale skin, and loss of hair on the extremity [18,21]. Rarely, it migrates to other joints. The ability of MRI to distinguish reflex sympathetic dystrophy from transient bone marrow edema is difficult, if not impossible. Some authors have suggested that these may represent stages of the same process. Clinically, however, these are decidedly distinct entities. MRI reveals diffuse, patchy bone marrow edema, which does not progress to the subchondral collapse seen in osteonecrosis. Epidermal and dermal edema patterns may also be seen in various stages of its evolution [22,23].
Infection Osteomyelitis Osteomyelitis exhibits increased signal intensity within the marrow on T2-weighted, STIR, and contrast-enhanced T1-weighted sequences. Low signal intensity predominates on T1-weighted sequences. Involvement may be diffuse or focal. It is often located adjacent to regions of skin ulceration, or involves areas commonly affected by hematogenous spread (ie, the metaphysis in a child) (Fig. 13). Because other causes of marrow edema may mimic
Fig. 14. Osteoarthritis. Coronal short tau inversion recovery image of an osteoarthritic knee shows degenerative changes with severe loss of cartilage in the medial compartment, meniscal subluxation, and bone marrow edema along both sides of the joint.
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osteomyelitis, supportive findings of infection should be sought, including overlying cortical destruction and an abscess or fistula extending to the bone at the site of the marrow abnormality.
nal intensity than muscle on T1-weighted sequences and high signal intensity on T2-weighted, STIR, and contrast-enhanced sequences [3,4]. The specific features of various bone and soft tissue tumors are discussed elsewhere in this issue.
Septic joint A septic joint is another source of abnormal marrow signal intensity. Features that favor a septic joint, although not pathognomonic, include a large joint effusion, bone marrow edema on both sides of the joint, and cartilage loss. These features unfortunately also may be seen with an inflammatory arthritis or neuropathic joint disease. Obtaining clinical history and communicating with the clinician are essential and if a septic joint is suspected, joint aspiration is indicated. Further discussion on marrow changes related to infection can be found elsewhere in this issue [24].
Tumors Most tumors involving the bone marrow are relatively vascular and contain a reasonably high fluid content. As such, they tend to demonstrate lower sig-
Arthritis Osteoarthritis Classic findings in osteoarthritis include cartilage thinning, osteophyte formation, subchondral cysts, or sclerosis, and at times loose bodies within the joint. The characteristic MRI features found in osteoarthritis include thinned, fissured, or absent articular cartilage, often with associated meniscal abnormalities; osseous changes, such as subchondral edema, sclerosis, and osteophyte formation; and a pattern of edema that is most intense in the subchondral regions and fades as it extends further from the joint (Fig. 14) [25]. The edema-like subchondral marrow signal is especially prominent in areas of deep cartilage fissuring or loss. In one study, histologic evaluation of marrow demonstrating this edema-like signal on MRIs revealed
Fig. 15. (A) Rheumatoid arthritis. Sagittal fat-saturated T1-weighted image of the knee after intravenous administration of Gd-DTPA reveals a moderate-sized low signal joint effusion that is surrounded by intensely enhancing, thickened synovial tissue. The synovial tissue is particularly prominent in the posterior recess of the knee and the suprapatellar bursa. (B) Axial gradient echo T2*-weighted image shows extensive high signal within the knee with synovial tissue isointense to joint effusion. Note the erosion involving the posterior aspect of the lateral femoral condyle, in a typical ‘‘bare area’’ of the joint (arrow).
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bone marrow necrosis, fibrosis, and trabecular abnormalities with a surprising paucity of actual bone marrow edema [26]. Although these histologic findings are similar to those seen with subchondral osteonecrosis, the recognition of other classic imaging abnormalities associated with osteoarthritis confirms this as the etiology. Inflammatory arthritides In the acute stages of an inflammatory arthritis, the patient presents with extensive synovitis and diffuse sympathetic subchondral edema, secondary to the increased metabolic activity and cartilage destruction in the adjacent joint. During the quiescent phase, if there are no osseous erosions, the bone may appear normal or the appearance may resemble the findings in osteoarthritis. MRI is able to confirm the clinical suspicion of an inflammatory arthropathy in most cases. Common findings include joint effusions and variable degrees of synovial thickening. Intravenous contrast is often needed to distinguish synovial inflammation from joint fluid, and is especially helpful in early cases where there is minimal synovial inflammation. Occasionally, the synovitis and bone marrow edema are not evident on fluid-weighted sequences and contrast administration then becomes invaluable in detecting the synovitis (Fig. 15) [27]. Additionally, MRI is more sensitive than radiographs in detecting early osseous erosions, in part because active bone erosions often demonstrate underlying bone marrow edema. In addition to these findings, the seronegative spondyloarthropathies demonstrate fluid or edemalike signal adjacent to enthesis on T2-weighted images. The seronegative arthropathies are more likely to exhibit multifocal entheseal involvement around a single joint than is rheumatoid arthritis. McGonagle et al [27] identified numerous vulnerable sites around the knee including the origin and insertion of the patellar tendon, medial and lateral collateral ligaments, semimembranosus tendon, iliotibial band, posterior cruciate ligament, and posterior capsule.
Summary MRI is clearly the imaging modality of choice for detecting and exploring joint, osseous, and soft tissue injuries in the lower extremity and throughout the musculoskeletal system. Its ability to detect and differentiate the various forms of marrow pathology is unrivaled, and as such it should be obtained early in the work-up of a patient with a suspected marrow
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abnormality. Additionally, the radiologist must be familiar with the MRI appearances of normal marrow and the most common types of marrow pathology if its diagnostic power is to be fully realized.
References [1] Vande Berg BC, Malghem J, Lecouvet FE, Maldague B. Magnetic resonance imaging of the normal bone marrow. Skeletal Radiol 1998;27:471 – 83. [2] Wilson AJ, Hodge JC, Pilgram TK, Kang EH, Murphy Jr. WA. Prevalence of red marrow around the knee joint in adults as demonstrated on magnetic resonance imaging. Acad Radiol 1996;3:550 – 5. [3] Vande Berg BC, Malghem J, Lecouvet FE, Maldague B. Classification and detection of bone marrow lesions with magnetic resonance imaging. Skeletal Radiol 1998;27:529 – 45. [4] Eustace S, Keogh C, Blake M, Ward RJ, Oder PD, Dimasi M. MR imaging of bone oedema: mechanisms and interpretation. Clin Radiol 2001;56:4 – 12. [5] Sanders TG, Medynski MA, Feller JF, Lawhorn KW. Bone contusion patterns of the knee at MR imaging: footprint of the mechanism of injury. Radiographics 2000;20:S135 – 51. [6] Hayes CW, Brigido MK, Jamadar DA, Propeck T. Mechanism-based pattern approach to classification of complex injuries of the knee depicted at MR imaging. Radiographics 2000;20:S121 – 34. [7] Palmer WE, Levine SM, Dupuy DE. Knee and shoulder fractures: association of fracture detection and marrow edema on MR images with mechanism of injury. Radiology 1997;204:395 – 401. [8] Resnick D, Goergen TG. Physical injury: concepts and terminology. In: Resnick D, editor. Diagnosis of bone and joint disorders. Philadelphia: WB Saunders; 2002. p. 2652 – 65. [9] Anderson MW, Greenspan A. Stress fractures. Radiology 1996;199:1 – 12. [10] Anderson MW, Ugalde V, Batt M, Greenspan A. Longitudinal stress fracture of the tibia: MR demonstration. J Comput Assist Tomogr 1996;20:836 – 8. [11] Anderson MW, Ugalde V, Batt M, Gacayan J. Shin splints: MR appearance in a preliminary study. Radiology 1997;204:177 – 80. [12] Anderson MW, Kaplan PA, Dussault RG. Adductor insertion avulsion syndrome (thigh splints): spectrum of MR imaging features. AJR Am J Roentgenol 2001; 177:673 – 5. [13] Posch TJ, Puckett ML. Marrow MR signal abnormality associated with bilateral avulsive cortical irregularities in a gymnast. Skeletal Radiol 1998;27:511 – 4. [14] Yamamoto T, Bullough PG. Subchondral insufficiency fracture of the femoral head and medial femoral condyle. Skeletal Radiol 2000;29:40 – 4. [15] Parker RK, Ross GJ, Urso JA. Transient osteoporosis of the knee. Skeletal Radiol 1997;26:306 – 9.
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[16] Resnick D, Sweet DE, Madewell JE. Osteonecrosis: pathogenesis, diagnostic techniques, specific situations, and complications. In: Resnick D, editor. Diagnosis of bone and joint disorders. Philadelphia: WB Saunders; 2002. p. 3599 – 685. [17] Resnick D, Goergen TG. Physical injury: concepts and terminology. In: Resnick D, editor. Diagnosis of bone and joint disorders. Philadelphia: WB Saunders; 2002. p. 2689 – 98. [18] Resnick D. Osteoporosis. In: Resnick D, editor. Diagnosis of bone and joint disorders. Philadelphia: WB Saunders; 2002. p. 1795 – 816. [19] Hayes CW, Conway WF, Daniel WW. MR imaging of bone marrow edema pattern: transient osteoporosis, transient bone marrow edema syndrome, or osteonecrosis. Radiographics 1993;13:1001 – 11. [20] Froberg PK, Braunstein EM, Buckwalter KA. Osteonecrosis, transient osteoporosis, and transient bone marrow edema. Radiol Clin North Am 1996;34:273 – 91. [21] Wambeek N, Munk PL, Lee MJ, Meek RN. Intra-articular regional migratory osteoporosis of the knee. Skeletal Radiol 2000;29:97 – 100. [22] Schweitzer ME, Mandel S, Schwartzman RJ, Knobler
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The knee: bone marrow abnormalities Michelle S. Barr, MD*, Mark W. Anderson, MD Department of Radiology, University of Virginia Health System, Charlottesville, VA 22908, USA
MRI is an invaluable tool for assessing the bone marrow. It is the most sensitive imaging modality for detecting marrow pathology and simultaneously provides a detailed depiction of the adjacent soft tissues. This article describes the appearance of normal and abnormal bone marrow in and around the knee as depicted with MRI.
Normal bone marrow Bone marrow is categorized into two types of tissue based on differences in their color at gross pathologic examination. The active, hematopoietic component is comprised mostly of erythrocytes and their precursors and is denoted as ‘‘red’’ marrow, whereas ‘‘yellow’’ (inactive) marrow is comprised primarily of fat. Each type of marrow displays a distinctive appearance on MRI based on the relative amounts of fat and water within it. Because fat tends toward very short T1 and moderately long T2 relaxation times, yellow marrow exhibits high signal intensity on T1-weighted and fast spin echo T2-weighted images, intermediate signal intensity on conventional T2-weighted images, and variable signal intensity on gradient echo images depending on the amount of trabecular bone present. On fat-saturated sequences, yellow marrow demonstrates relatively homogeneous signal intensity that is lower than that of muscle. Contrast administration results in only minimal alteration in the yellow marrow signal intensity [1]. The signal characteristics of red marrow stem from its higher percentage of water (40% versus 15% in
* Corresponding author. E-mail address: [email protected] (M.S. Barr).
yellow marrow). On T1-weighted spin echo and fast spin echo imaging, it exhibits lower signal intensity than fat, whereas demonstrating higher signal intensity than that of muscle. Red marrow demonstrates intermediate to high signal intensity on short tau inversion recovery (STIR) or fat-suppressed T2weighted images and variable signal characteristics on gradient echo images (Fig. 1). Enhancement of red marrow is minimal in adults but can be quite marked in children [1].
Normal marrow conversion The normal distribution of red and yellow marrow varies with age. In utero and through childhood, hematopoietic marrow predominates. Shortly before birth, marrow in the distal phalanges converts from red to yellow. This process normally progresses with age from distal to proximal within the appendicular skeleton. Not only does bone marrow conversion progress from the most distal to the most proximal portions of the skeleton, but it also progresses in a predictable fashion within each bone. Within a long bone, the conversion from red to yellow marrow starts in the diaphysis, in the region of the central diaphyseal vessels, and extends both proximally and distally toward each end. The epiphysis is different because it converts to fatty marrow early in infancy when it begins to ossify. Low signal intensity marrow within an epiphysis on T1-weighted images is abnormal if it is seen later than 6 months after the ossification center first appeared [1]. Yellow marrow occupies most of the diaphysis in a child’s long bone during the first decade of life, and is identified on T1-weighted images by its relatively bright fat. Conversion from red to yellow marrow
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Fig. 1. (A) Normal marrow. Coronal T1-weighted image shows a normal adult marrow pattern. Note the metadiaphyseal hematopoietic marrow, which is slightly hyperintense to muscle and sharply marginated at the old physeal plate (arrow). (B) Coronal short tau inversion recovery image highlights the hyperintense hematopoietic marrow adjacent to the dark, saturated fat of the yellow marrow elsewhere in the bones.
continues to occur throughout the second decade, although some residual red marrow is retained in the proximal humeral and femoral metaphyses. The adult marrow pattern is present by 25 years of age. At this point, red marrow is found predominantly in the axial skeleton, sternum, ribs, and proximal metaphyses of the femora and humeri (Fig. 2). Marrow conversion slows at this point and becomes
dependent on variables, such as gender, nutritional status, obesity, activity, medications, smoking, and age [1 – 3]. Reconversion of yellow to red marrow occurs in areas where sinusoidal networks and perivascular reticular cells can appear rapidly: metaphyseal and metaphyseal equivalent regions, subchondral epiphyseal areas, and diaphyseal endosteal spaces. This
Fig. 2. Adult marrow pattern. Coronal T1-weighted MRI of the pelvis demonstrates red marrow within the pelvis and proximal femurs with fatty marrow in the femoral heads and greater trochanters.
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pattern is the reverse of red to yellow conversion in that reconversion to red marrow begins in the ends of the bones and progresses toward the mid-diaphyses. Difficulties may arise when attempting to distinguish normal red marrow from marrow pathology. There are several imaging features that favor the diagnosis of hematopoietic marrow. Most types of marrow pathology result in signal intensity that is lower than that of skeletal muscle or intervertebral disk on T1-weighted images, whereas hematopoietic marrow demonstrates signal intensity that is slightly higher than that of skeletal muscle or disk on T1weighted images (owing to the relatively high amount of fat present even in red marrow). Other features of red marrow include signal intensity that parallels the signal intensity of other areas of known hematopoietic marrow, bilateral symmetry, scattered foci of fatty signal within the region of concern, and an abrupt margination at the level of a closed physis (see Fig. 1) [1,2]. In some adults, however, red marrow also may extend into the epiphyseal regions. Although normalappearing bone marrow on MRI does not definitively exclude the possibility of disease, a thorough understanding of the MRI appearance of normal hematopoietic marrow allows for an improved ability to distinguish the normal from the pathologic.
Marrow pathology
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pattern within the marrow that is most conspicuous on fat-saturated T2 or STIR images (Fig. 3). Direct trauma to the bone can produce a focal contusion, but these most often result from one bone impacting on another. The ‘‘kissing contusions’’ often seen with anterior cruciate ligament tears are a classic example of this type of injury (Fig. 4). Evaluation of a contusion pattern often reveals the mechanism of injury and predicts associated soft tissue pathology. The marrow abnormalities may also prompt a careful search for less easily detected avulsive injuries that may result in joint instability necessitating surgical intervention [5,6]. Acute avulsive injuries Distraction injuries usually occur in response to rotational, varus, or valgus stress on a joint and often result in a small avulsion fracture related to a tendinous, ligamentous, or capsular attachment on the bone. The associated marrow edema is much less extensive than the edema seen with an impaction injury because cortical rather than medullary bone is involved [4 – 7]. The avulsed fragment can be very difficult to detect by MRI because there is usually a disproportionate amount of edema and hemorrhage in the adjacent soft tissue that may mask the small osseous fragment. A small avulsion fragment is often demonstrated better on conventional radiographs (Fig. 5).
Entities that affect the bone marrow are varied and include trauma, osteonecrosis, infection, tumors, arthritides, and metabolic disorders. Bone marrow typically demonstrates a similar response, however, regardless of the insult: increased fluid content in the form of edema, hemorrhage, pus, or tumor [3,4]. With this limited repertoire, it seems nearly hopeless that MRI could provide any specificity when attempting to differentiate between these varied etiologies, but a systematic approach of analyzing the pattern of marrow pathology and associated abnormalities often helps to limit the differential, or even arrive at a specific diagnosis.
Trauma Acute impaction injuries An acute impaction force on a bone results in marrow hemorrhage and edema, disruption of trabeculae, and interstitial fluid leakage within the marrow space. On MRI, these bone bruises (contusions) are identified by the vague, geographic, edema-like
Fig. 3. Bone contusion. Coronal short tau inversion recovery image demonstrates vague geographic edema in the lateral tibial condyle compatible with a bone marrow contusion.
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that is exacerbated with activity and relieved with rest. Palpation often reveals tenderness and soft tissue swelling over the site of osseous damage [8,9]. MRIs reveal a spectrum of findings from periosteal edema alone, to progressively severe marrow edema, to a hypointense fracture line in cancellous or cortical bone (Fig. 6). The fracture line is most often of a transverse or oblique orientation within a long bone, but longitudinal stress fractures also have been described [10]. Chronic avulsive injuries
Fig. 4. Anterior cruciate ligament tear contusion pattern. Sagittal T2-weighted fat-saturated MRI demonstrates the ‘‘kissing contusion’’ pattern often seen with anterior cruciate ligament tears. Subchondral edema-like signal is present in the lateral femoral condyle and the posterolateral tibial plateau.
Fatigue and insufficiency fractures Fatigue and insufficiency fractures demonstrate similar radiographic and MRI findings. Fatigue fractures develop when abnormal stress is applied to normally mineralized bone, whereas insufficiency fractures result from normal activities applied to weakened bone. Clinically, these injuries induce pain
‘‘Shin splints’’ refers to a syndrome of activityrelated lower leg pain that has long been thought to be related to a traction periostitis of the calf muscle along the posteromedial tibia. In addition to the expected periosteal edema or fluid, MRI has also revealed marrow edema and even cortical signal abnormalities that indicate osseous stress injuries of varying degrees [8,11]. Thigh splints (adductor insertion avulsion syndrome) is a similar condition and refers to activityrelated groin or thigh pain that is thought to be related to the pull of the adductor tendons on the proximal to mid femoral shaft. As with shin splints, MRI reveals a spectrum of osseous injury from periosteal edema or fluid to varying degrees of marrow edema (Fig. 7) [12]. The avulsive cortical irregularity syndrome (cortical desmoid) occurs along the posterior margin of the distal femur and in some cases can be difficult to distinguish from a paraosteal osteosarcoma. The MRI appearance may also be confusing. Posch and Puckett
Fig. 5. (A) Avulsion fracture. Coronal short tau inversion recovery image of the knee reveals a small cortical avulsion fracture (Segond fracture) along the lateral tibial plateau (black arrow). Compare the prominence of the soft tissue edema with the paucity of marrow edema (white arrow). (B) Anteroposterior radiograph of the knee. The fracture fragment is seen more easily.
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Fig. 6. Stress fracture. Coronal short tau inversion recovery image of the proximal lower legs in a child with left lower leg pain reveals a hypointense fracture line extending horizontally through an area of extensive marrow edema in the proximal left tibia. Note also the marked periosteal thickening and soft tissue edema in that region.
[13] describe the features that favor a benign entity: bilateral symmetry (even if the contralateral side is asymptomatic); edema with enhancement at the base of the irregularity, which remains outside of the medullary canal and along the outer confines of the cortex; clinical history of a physically active young child; and minimal uptake on nuclear medicine bone scan. The location of the lesion is characteristic, lying at the medial ridge of the linea aspera just superior to the adductor tubercle (Fig. 8). This site suggests a relationship to the insertion of the adductor magnus
tendon or the origin of the medial head of the gastrocnemius muscle. Spontaneous osteonecrosis As its name implies, spontaneous osteonecrosis is a condition that affects the knee and results in an area of subchondral necrosis. Although long thought to represent a form of primary osteonecrosis, recent studies have concluded that this lesion is actually a subchondral insufficiency fracture that results in a
Fig. 7. Thigh splints. Coronal short tau inversion recovery image of the proximal thighs in this young track runner demonstrates foci of marrow edema along the medial endosteum of the proximal femoral shafts. The changes are slightly worse in the right femur, which also displays mild periostitis (arrow).
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different location in the medial femoral condyle (weight-bearing surface), and a unique MRI appearance. Radiographs are often normal, even though the pain is severe, and the patient is unable to ambulate. On MRI, extensive edema-like signal is seen in the medial femoral condyle along with a linear subchondral focus of low signal intensity that represents the insufficiency fracture (Fig. 9).
Osteonecrosis Medullary infarction
Fig. 8. Cortical irregularity of the distal femur. Sagittal gradient echo T2*-weighted image of the knee shows a welldefined, rounded, intracortical lesion along the posterior metaphysis of the distal femur. Note the edema along the surface of the bone and within the adjacent soft tissues.
devitalized segment of bone between the fracture line and overlying articular cartilage [14]. This most likely explains why this entity can usually be differentiated from osteochondritis dissecans (described later). Spontaneous osteonecrosis typically has an older age of onset (most commonly a middle-aged woman), an abrupt onset of symptoms, a
Several factors are known to predispose to the development of focal areas of medullary infarction. These include the use of exogenous corticosteroids; increased production of endogenous steroids (eg, Cushing’s syndrome); alcohol abuse; pancreatitis; vasculitis; trauma; radiation; hemodialysis; and hemoglobinopathies (sickle cell anemia, thalassemia, polycythemia). Some cases are idiopathic [4,14]. Medullary infarcts result in geographic areas of ischemic and devitalized marrow that produce a characteristic MRI appearance: a geographic focus of typically heterogeneous signal within the marrow that is surrounded by characteristic low signal intensity, serpentine border on T1-weighted images. This border often demonstrates a classic double-line sign on
Fig. 9. (A) Spontaneous osteonecrosis. Coronal short tau inversion recovery (STIR) image of the knee demonstrates extensive edema within the medial femoral condyle extending to the intercondylar notch. (B) Sagittal STIR image of the knee reveals a linear subchondral fracture within the marrow edema (arrow).
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Fig. 10. (A) Medullary infarcts. Sagittal T1-weighted image of the knee demonstrates the classic undulating serpentine border of medullary infarct in the proximal tibia that is pathognomonic for osteonecrosis. Note the central fat, characteristics for this lesion. (B) Sagittal T1-weighted MRI of the knee reveals a second infarct in this same patient in a more subchondral location of the medial femoral condyle.
T2-weighted images that manifests as an inner margin of high signal intensity surrounded by an outer rim of low signal intensity [15,16]. This is one of the few medullary lesions that usually contain some central fat (Fig. 10). In the early stages of an acute medullary infarct, only marrow edema may be present, making it difficult to differentiate this from other types of pathology. Similarly, ischemic foci may present as areas of edema-like signal within the marrow, but unlike a true medullary infarct, these tend to be transitory. Osteochondritis dissecans A special form of subchondral osteonecrosis is termed osteochondritis dissecans. This entity is most frequently seen in adolescents and young adults and refers to fragmentation, and often separation, of a portion of subchondral bone, typically along the lateral aspect of the medial femoral condyle. The cause of this lesion is uncertain but it is thought to result from repetitive trauma that produces shear forces across the cartilage. Radiographic findings include a geographic, subchondral lucency along the non – weight-bearing surface of the medial femoral condyle [17].
MRI plays an important role in detecting the lesion if plain films are normal. A crescentic or ovoid focus of subchondral signal abnormality is evident (Fig. 11). The primary concern when evaluating a focus of osteochondritis dissecans is whether the fragment of subchondral bone is unstable (ie, at risk of evolving into a displaced loose body in the joint), in which case it likely requires operative intervention. Several MRI features have been shown to be suggestive of an unstable fragment. These include fluid tracking between the fragment and host bone, cystic foci at that same interface, or a 5-mm or larger defect in the overlying cartilage. MR arthrography can be used in this setting to confirm that a fragment is truly unstable by demonstrating intra-articular gadolinium tracking between the fragment and host bone (Fig. 12). Transient bone marrow edema syndrome (transient osteoporosis) Transient bone marrow edema syndrome (also known as transient osteoporosis) was first described in the hip. Originally reported in women during their third trimester of pregnancy, this entity also has been
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Fig. 11. Osteochondritis dissecans. Coronal short tau inversion recovery image of the knee. An osseous fragment has partially detached from the lateral non – weight-bearing aspect of the medial femoral condyle (arrowhead ). Cystic changes and some joint fluid are present between the osseous fragment and femoral condyle.
shown to be common in men. Its exact cause is uncertain but several authors have postulated that local trauma, reflex sympathetic dystrophy, bone marrow edema, and insufficiency fractures may actually represent successive stages of a process that could ultimately culminate in osteonecrosis [18].
Affected patients present with an acute onset of pain, usually not associated with trauma. Within 2 to 4 weeks of the initial symptoms, radiographs may reveal femoral head and neck osteopenia with marked indistinctness of the subchondral cortical bone [19]. MRI findings include diffuse, nonfocal, edema (low signal on T1-weighted images and high signal on T2-weighted or STIR sequences) [19,20]. In the knee, the lateral femoral condyle is usually involved, although involvement of the medial femoral condyle and tibial plateau has also been described [15,21]. Resolution of pain and edema usually takes place within 6 to 12 months. Long-term sequelae do not occur. The ability to distinguish transient bone marrow edema syndrome from other entities is difficult and is often a diagnosis of exclusion, with osteonecrosis, reflex sympathetic dystrophy, insufficiency fractures, or trauma constituting other differential possibilities. Reflex sympathetic dystrophy The exact cause of reflex sympathetic dystrophy is unclear but it is believed to represent sequelae from hyperactivity of the sympathetic nervous system. The most common of the varied entities producing this syndrome are trauma, hemiplegia, and myocardial infarction. Reflex sympathetic dystrophy most often affects the upper extremities, and in many cases occurs after
Fig. 12. Osteochondral lesion. MR arthrogram. Coronal fat-saturated T1-weighted MR arthrogram reveals an unstable fragment with gadolinium tracking between the fragment and host bone.
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Fig. 13. (A) Osteomyelitis. Radiograph of the left femur reveals a focal ill-defined lytic lesion in the lateral metaphysis of the digital femur and an aggressive, interrupted periostitis. This proved to represent bacterial osteomyelitis on biopsy. (B) Coronal T1-weighted MRI of the femur reveals disruption of the cortex in the lateral metaphysis of the distal left femur with effacement of the normal fat signal adjacent to the bone (arrow). (C) Coronal short tau inversion recovery image of the femur better demonstrates associated signal abnormality in the marrow and edema involving the soft tissues.
a recent episode of trauma. It results in circulatory changes and may progress to muscle atrophy, contractures, pale skin, and loss of hair on the extremity [18,21]. Rarely, it migrates to other joints. The ability of MRI to distinguish reflex sympathetic dystrophy from transient bone marrow edema is difficult, if not impossible. Some authors have suggested that these may represent stages of the same process. Clinically, however, these are decidedly distinct entities. MRI reveals diffuse, patchy bone marrow edema, which does not progress to the subchondral collapse seen in osteonecrosis. Epidermal and dermal edema patterns may also be seen in various stages of its evolution [22,23].
Infection Osteomyelitis Osteomyelitis exhibits increased signal intensity within the marrow on T2-weighted, STIR, and contrast-enhanced T1-weighted sequences. Low signal intensity predominates on T1-weighted sequences. Involvement may be diffuse or focal. It is often located adjacent to regions of skin ulceration, or involves areas commonly affected by hematogenous spread (ie, the metaphysis in a child) (Fig. 13). Because other causes of marrow edema may mimic
Fig. 14. Osteoarthritis. Coronal short tau inversion recovery image of an osteoarthritic knee shows degenerative changes with severe loss of cartilage in the medial compartment, meniscal subluxation, and bone marrow edema along both sides of the joint.
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osteomyelitis, supportive findings of infection should be sought, including overlying cortical destruction and an abscess or fistula extending to the bone at the site of the marrow abnormality.
nal intensity than muscle on T1-weighted sequences and high signal intensity on T2-weighted, STIR, and contrast-enhanced sequences [3,4]. The specific features of various bone and soft tissue tumors are discussed elsewhere in this issue.
Septic joint A septic joint is another source of abnormal marrow signal intensity. Features that favor a septic joint, although not pathognomonic, include a large joint effusion, bone marrow edema on both sides of the joint, and cartilage loss. These features unfortunately also may be seen with an inflammatory arthritis or neuropathic joint disease. Obtaining clinical history and communicating with the clinician are essential and if a septic joint is suspected, joint aspiration is indicated. Further discussion on marrow changes related to infection can be found elsewhere in this issue [24].
Tumors Most tumors involving the bone marrow are relatively vascular and contain a reasonably high fluid content. As such, they tend to demonstrate lower sig-
Arthritis Osteoarthritis Classic findings in osteoarthritis include cartilage thinning, osteophyte formation, subchondral cysts, or sclerosis, and at times loose bodies within the joint. The characteristic MRI features found in osteoarthritis include thinned, fissured, or absent articular cartilage, often with associated meniscal abnormalities; osseous changes, such as subchondral edema, sclerosis, and osteophyte formation; and a pattern of edema that is most intense in the subchondral regions and fades as it extends further from the joint (Fig. 14) [25]. The edema-like subchondral marrow signal is especially prominent in areas of deep cartilage fissuring or loss. In one study, histologic evaluation of marrow demonstrating this edema-like signal on MRIs revealed
Fig. 15. (A) Rheumatoid arthritis. Sagittal fat-saturated T1-weighted image of the knee after intravenous administration of Gd-DTPA reveals a moderate-sized low signal joint effusion that is surrounded by intensely enhancing, thickened synovial tissue. The synovial tissue is particularly prominent in the posterior recess of the knee and the suprapatellar bursa. (B) Axial gradient echo T2*-weighted image shows extensive high signal within the knee with synovial tissue isointense to joint effusion. Note the erosion involving the posterior aspect of the lateral femoral condyle, in a typical ‘‘bare area’’ of the joint (arrow).
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bone marrow necrosis, fibrosis, and trabecular abnormalities with a surprising paucity of actual bone marrow edema [26]. Although these histologic findings are similar to those seen with subchondral osteonecrosis, the recognition of other classic imaging abnormalities associated with osteoarthritis confirms this as the etiology. Inflammatory arthritides In the acute stages of an inflammatory arthritis, the patient presents with extensive synovitis and diffuse sympathetic subchondral edema, secondary to the increased metabolic activity and cartilage destruction in the adjacent joint. During the quiescent phase, if there are no osseous erosions, the bone may appear normal or the appearance may resemble the findings in osteoarthritis. MRI is able to confirm the clinical suspicion of an inflammatory arthropathy in most cases. Common findings include joint effusions and variable degrees of synovial thickening. Intravenous contrast is often needed to distinguish synovial inflammation from joint fluid, and is especially helpful in early cases where there is minimal synovial inflammation. Occasionally, the synovitis and bone marrow edema are not evident on fluid-weighted sequences and contrast administration then becomes invaluable in detecting the synovitis (Fig. 15) [27]. Additionally, MRI is more sensitive than radiographs in detecting early osseous erosions, in part because active bone erosions often demonstrate underlying bone marrow edema. In addition to these findings, the seronegative spondyloarthropathies demonstrate fluid or edemalike signal adjacent to enthesis on T2-weighted images. The seronegative arthropathies are more likely to exhibit multifocal entheseal involvement around a single joint than is rheumatoid arthritis. McGonagle et al [27] identified numerous vulnerable sites around the knee including the origin and insertion of the patellar tendon, medial and lateral collateral ligaments, semimembranosus tendon, iliotibial band, posterior cruciate ligament, and posterior capsule.
Summary MRI is clearly the imaging modality of choice for detecting and exploring joint, osseous, and soft tissue injuries in the lower extremity and throughout the musculoskeletal system. Its ability to detect and differentiate the various forms of marrow pathology is unrivaled, and as such it should be obtained early in the work-up of a patient with a suspected marrow
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abnormality. Additionally, the radiologist must be familiar with the MRI appearances of normal marrow and the most common types of marrow pathology if its diagnostic power is to be fully realized.
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[16] Resnick D, Sweet DE, Madewell JE. Osteonecrosis: pathogenesis, diagnostic techniques, specific situations, and complications. In: Resnick D, editor. Diagnosis of bone and joint disorders. Philadelphia: WB Saunders; 2002. p. 3599 – 685. [17] Resnick D, Goergen TG. Physical injury: concepts and terminology. In: Resnick D, editor. Diagnosis of bone and joint disorders. Philadelphia: WB Saunders; 2002. p. 2689 – 98. [18] Resnick D. Osteoporosis. In: Resnick D, editor. Diagnosis of bone and joint disorders. Philadelphia: WB Saunders; 2002. p. 1795 – 816. [19] Hayes CW, Conway WF, Daniel WW. MR imaging of bone marrow edema pattern: transient osteoporosis, transient bone marrow edema syndrome, or osteonecrosis. Radiographics 1993;13:1001 – 11. [20] Froberg PK, Braunstein EM, Buckwalter KA. Osteonecrosis, transient osteoporosis, and transient bone marrow edema. Radiol Clin North Am 1996;34:273 – 91. [21] Wambeek N, Munk PL, Lee MJ, Meek RN. Intra-articular regional migratory osteoporosis of the knee. Skeletal Radiol 2000;29:97 – 100. [22] Schweitzer ME, Mandel S, Schwartzman RJ, Knobler
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