F. M. Vanhoenacker, MD, PhD P. Van Dyck, MD
J. L. Gielen, MD, PhD
Department of Radiology, University Hospital Antwerp, Wilrijkstraat 10, 2650 Edegem, Belgium
W. Geyskens, MD
Algemeen Ziekenhuis Maria Middelares, Hospitaalstraat 17, 9100 Sint-Niklaas, Belgium
C O N T E N T S
6.1 Introduction 73
6.2 Defi nition and Classifi cation 74
6.3 Pathogenesis of Bone Marrow Edema in Sports Injuries 74
6.3.1 Acute Traumatic Lesions 74 6.3.1.1 Impaction Injuries 74 6.3.1.2 Avulsive Injuries 74 6.3.1.3 Complex Patterns 75 6.3.2 Chronic Traumatic Lesions (Repetitive Trauma) 79 6.3.2.1 Fatigue Fractures 79 6.3.2.2 Chronic Avulsive Injuries 79 6.3.2.3 Altered Biomechanics and BME 79 6.3.3 Lesions of Unknown Pathogenesis 79 6.3.3.1 Bone Marrow Edema Syndrome 79 6.3.3.2 Bone Marrow Edema in Long Distance
Runners 80
6.3.3.3 Subchondral Insuffi ciency Fracture 80 6.4 Histopathological Correlation 80 6.5 Clinical Signifi cance 81
6.6 Natural Evolution 81
6.6.1 Follow-up of Acute Traumatic Bone Marrow
Edema 81
6.6.2 Follow-up of Chronic Traumatic Lesions 82 6.6.3 Follow-up of BMES 82
6.7 Conclusion 82
Things to Remember 83 References 83
Bone Marrow Edema in Sports Injuries: 6
General Concept
Filip M. Vanhoenacker, Pieter Van Dyck, Jan L . Gielen, and Wim Geyskens
6.1
Introduction
Macroscopically, living bone consists of compact bone and cancellous bone.
Cancellous bone, also designated as trabecular or spongy bone is a honeycomb of large cavities with an internal latticework of bars and plates (trabeculae).
Compact bone is usually limited to the cortices of mature bones (cortical bone) and is most important in providing the strength of bone.
Cancellous bone lies in the inner part of the bone, and particularly, in case of the long bones, within their expanded ends (metaphyses and epiphyses).
Cancellous bone gives additional strength to cortical bone and supports the bone marrow (Soames 1995).
Before the advent of Magnetic Resonance Imag- ing (MRI), trauma to the trabecular bone was diffi - cult to assess on radiological examinations, because
Box 6.1. MRI
● Gold standard for evaluation of traumatic bone marrow edema
● May reveal associated soft tissue lesions or intra-articular pathology
● Fat suppression techniques are most valuable
Box 6.2. Standard radiography / (multidetector)-CT
● No role for depiction of bone marrow edema
● Main role is detection of (subtle) avulsion fractures
the subchondral lamella, representing focal cancel- lous impaction (possible patterns are geographic, crescent and linear). Those lesions can be designated as type IIb lesions.
Multidetector CT will of course pick up the focal depressions / osteochondral fractures (III) and prob- ably also the subchondral impactions (IIb).
6.3
Pathogenesis of Bone Marrow Edema in Sports Injuries
Traumatic bone marrow edema (bruise) is most fre- quent and the underlying mechanism may be either acute or chronic.
Variable incidences have been published but edema is often encountered in acute trauma (pub- lished incidences vary from 27% to 72%).
A minority of the studies of acute injuries (knee and ankle) will show bruising only without associ- ated injuries.
6.3.1
Acute Traumatic Lesions
Bone marrow edema is frequently encountered on MRI after an injury to the musculoskeletal system (Sanders et al. 2000). These osseous injuries may result from several forces acting on the joint. In general, compressive forces vs traction forces will infl uence the extent of BME edema around the joint (Hayes et al. 2000).
6.3.1.1
Impaction Injuries
Focal bruise may result from direct trauma to the bone (Fig. 6.1), but often a specifi c pattern of bone marrow changes on adjacent bones occurs due to impaction of one bone on another.
Impaction type of BME is extensive and will involve a broad surface of the involved bony structures.
6.3.1.2
Avulsive Injuries
Distraction injuries are usually due to valgus, varus or rotational stress on a joint, resulting in a small the overlying cortex is often intact (Mandalia et al.
2005). This chapter will review bone marrow edema due to sports injuries, with special emphasis on the mechanisms of trauma, clinical signifi cance and nat- ural evolution.
6.2
Defi nition and Classifi cation
‘Bone bruise’ was described for the fi rst time in the knee by Yao and Lee in 1988. The term “bruise”
indicates the traumatic origin of these bone marrow changes. It was defi ned as region of T2-hyperin- tensity in the absence of frank osseous fracture or subchondral cysts. MRI examination showed intra- osseous areas, hyperintense on T2-weighted/STIR images and (to a lesser degree) hypo-intense on T1- images, in acutely injured joints with no abnormali- ties on plain radiographs. The use of an intermedi- ate TE in FS T2-weighted images has an additional value in demonstrating underlying cartilage lesions.
Since then bone bruise, bone contusion and occult fracture have been used interchangeably. Most authors use the term occult when standard radio- graph shows no abnormalities but with the advent of multidetector CT with submillimetric multiplanar reconstructions we will probably have to redefi ne
‘occult’. In radiologically overt fractures one can speak of accompanying bruise in the surrounding cancellous bone.
Several classifi cation systems have been proposed.
Most authors agree on differentiation between reticu- lar and geographic/demarcated pattern. Others stress the importance of the location (subchondral versus at distance of joint space). Costa-Paz et al. (2001) proposes the following classifi cation: type I: diffuse, often reticular, alterations of the medullary compo- nent, distant from the subjacent articular surface;
type II (a and b) localized/geographic signal (mostly convex margins towards normal marrow) with conti- guity to articular surface; type III: (slight) disruption or depression of the normal contour of the cortical surface/ subchondral lamella, often associated with type II lesion (small osteochondral compression fractures).
In a type II lesion compared to type I, the impact is more focally concentrated. Some authors describe subchondral impaction fractures as an additionally marked hypo-intense area on T1-WI directly beneath
avulsion fracture related to a tendinous, ligamentous or capsular attachment on the bone.
Because the cortical bone is involved rather than the trabecular bone, the resulting “avulsion BME pat- tern” is much less extensive than in impaction inju- ries.
Moreover, the avulsed bone fragment may be very diffi cult to detect on MRI (Fig. 6.2a). In most instances, a small avulsion is far better demonstrated on conventional radiographs (Fig. 6.2b) or CT.
6.3.1.3
Complex Patterns
In most clinical situations, this rigorous distinction between ”pure impaction type injuries” and “avulsive type injuries” is artifi cial, because both types will be seen in a single joint after acute traumatic inju- ries. Generally, the impaction type of bone marrow edema will be encountered on the entry site of the force acting on a joint, whereas a distraction type of bone marrow edema will be seen on the exit site of the force. Although avulsive type bone marrow edema is less extensive than the impaction type, the
Fig. 6.1. Bone marrow edema (BME) due to a direct blow (impaction type BME). Sagittal fat suppressed FSE T2-weighted image of the knee shows extensive BME at the anterior aspect of the distal femur
Fig. 6.2a,b. Typical example of an avulsion fracture and associated BME (avulsion type BME). a Coronal fat suppressed FSE T2-weighted image of the right knee shows only minor focal BME at the lateral aspect of the tibia. The bony avulsion fracture is barely visible. b Standard radiograph (AP spot view) clearly shows an avulsion fracture (Segond fracture)
a b
former is usually the witness of underlying ligamen- tous sprain.
These soft tissue lesions are often less conspicu- ous than the bruises, though they are more impor- tant, at least in the short term follow-up, for stability reasons.
Indeed, sprain of the supporting structures of the joint may cause instability, if not recognised and appropriately treated.
Moreover, bone marrow edema around a joint is usually the result of a combination of multiple forces (and not of a single force), which all have a certain amplitude and direction. The impact of these forces may differ with the position of the joint at the moment of the trauma (e.g. degree of fl exion, varus, valgus....).
Certain combinations of forces are known to cause a specifi c injury.
Systematic analysis of the BME-pattern, together with the associated soft tissue changes can often reveal the specifi c mechanism of injury.
In this regard, the pattern and distribution of BME represents a ‘footprint’ of the mechanism of acute trauma (Sanders et al. 2000).
In the knee for example, classic patterns which are encountered in sports injuries are the pivot shift injury (Figs. 6.3 and 6.4), the hyperextension injury (Fig. 6.5), the clip injury (Fig. 6.6), dashboard injury (Fig. 6.7) and (transient) lateral patellar dislocation (Fig. 6.8).
Pivot shift injury which occurs when valgus load is applied to the knee in various states of fl exion, combined with external rotation of the tibia or inter- nal rotation of the femur, will result in disruption of ACL. Resultant anterior subluxation of the tibia will cause impaction of the lateral femoral condyle against the posterolateral margin of the lateral tibial plateau. Therefore, BME will be present in the poste- rior aspect of the lateral tibial plateau and the middle portion of the lateral femoral condyle. Associated bone bruising at the posterior lip of the medial tibial plateau may be the result of contrecoup forces due to valgus forces (Kaplan et al. 1999). According to others this medial-sided bone bruise is attributed to avulsion at the semimembranosus attachment (Chan et al. 1999). Concomitant soft tissue injuries of the pivot shift injury are medial collateral liga- ment (MCL) lesions, lesion of the posterior horn of the lateral and medial meniscus or a tear at the pos- terior joint capsule.
Hyperextension injury results in a kissing contu- sion pattern in the anterior aspect of the distal femur and proximal tibia. Associated soft tissue lesions may include ACL or PCL tears or meniscal lesions.
The classic bone contusion pattern seen after lat- eral patellar dislocation includes involvement of the anterolateral aspect of the lateral femoral condyle and the inferomedial aspect of the patella.
Associated soft tissue injuries include sprain or disruption of the medial soft tissue restraints (medial
Fig. 6.3a,b. Pivot shift injury due to a combination of external rotation of the tibia, valgus stress and fl exion in a skier. These manoevers stress the anterior cruciate ligament (ACL), which is prone to rupture. a Midsagittal fat suppressed FSE T2-weighted image of the right knee shows complete disruption of the ACL. b Sagittal fat suppressed FSE T2-weighted image of the right knee. Due to anterior subluxation of the tibia relative to the femur, impaction occurs between the posterolateral margin of the lateral tibial plateau and the lateral femoral condyle, resulting in extensive impaction type BME
a b
retinaculum, medial patellofemoral ligament and the medial patellotibial ligament).
Clip injury occurs when pure valgus stress is applied to the knee while the knee is in mild fl exion.
BME is most prominent in the lateral femoral condyle due to impaction forces, whereas a second smaller area of edema may be present in the medial femoral condyle secondary to avulsive forces at the insertion of the MCL.
Dashboard injury occurs when a posteriorly directed force is applied to the anterior aspect of the
proximal tibia while the knee is in a fl exed position.
This will result in BME at the anterior aspect of the tibia and occasionally at the posterior surface of the patella. Associated soft tissue injuries are disruption of the posterior cruciate ligament and posterior joint capsule.
Failure of this pattern approach revealing the underlying mechanism of trauma may be due to several factors, including insuffi cient trauma, mas- sive injury, or pre-existing osteoarthritis associated with BME (Felson et al. 2001; Vanhoenacker et al.
Fig. 6.4a–c. Another pivot shift injury in a soccer player with associated BME at the posteromedial corner of the knee. a Sagittal fat suppressed FSE T2-weighted image of the lateral aspect of the right knee. BME at the postero- lateral aspect of the tibia and corresponding BME at the middle part of the lateral femur condyle (with associated focal cortical depression). b Midsagittal fat suppressed FSE T2-weighted image of the right knee shows com- plete disruption of the ACL. c Sagittal fat suppressed FSE T2-weighted image of the medial aspect of the right knee.
Note also BME at the posteromedial aspect of the tibia near the distal of the semimembranosus tendon. According to some authors, this lesion represents a contre-coup impac- tion lesion. According to others, however, this lesion repre- sents a traction injury at the posteromedial corner of the knee due to external rotation of the knee
a
c
b
Fig. 6.6. Clip injury in a soccer player. Coronal fat suppressed FSE T2 weighted image of the left knee shows a large area of BME involving the lateral femoral condyle. Minimal edema is noted within the medial femoral condyle near the proximal attachment of the MCL. There is partial disruption of the MCL
Fig. 6.5. Hyperextension trauma in a soccer player. Midsagit- tal fat suppressed FSE T2-weighted image of the right knee.
Severe hyperextension of the knee can result in the impac- tion of the anterior aspect of the femoral condyle against the anterior aspect of the tibial plateau. At the posterior aspect of the knee (distraction site), there is rupture of the posterior cruciate ligament and indistinct outline of the posterior joint capsule
Fig. 6.7a,b. Dashboard injury. a Sagittal fat suppressed FSE T2-weighted image showing BME at the proximal tibia. b Axial fat suppressed FSE T2-weighted image demonstrating focal BME at the proximal tibia as well as an associated superfi cial infrapatellar bursitis
a b
2005), usually encountered in older sporters. More- over, accelerated osteoarthritis is more prevalent in sporters than in the general population, due to previ- ous repetitive trauma.
6.3.2
Chronic Traumatic Lesions (Repetitive Trauma) Besides pure acute traumatic causes of BME, BME may result from repetitive or chronic trauma in sports activities.
6.3.2.1
Fatigue Fractures
Chronic stress on a normally mineralized bone may result in a spectrum of MRI fi ndings ranging from periosteal edema over severe marrow edema to a hypo-intense fracture line in cancellous or cortical bone. This item will be described more in detail in Chap. 7.
6.3.2.2
Chronic Avulsive Injuries
Typical examples of chronic avulsive injuries include shin splints (traction periostitis of the calf muscles along the posteromedial tibia), thigh splints (distal
adductor insertion avulsion syndrome) and adduc- tor/gracilis syndrome.
Apart from periostal edema, MRI may also reveal BME and cortical signal abnormalities.
6.3.2.3
Altered Biomechanics and BME
Altered biomechanics due to certain sports activi- ties (jogging, golf, etc.) may induce physiologic bone response to repeated stress. MRI may reveal bone marrow edema in these cases, which may not neces- sarily correspond with severe trauma (Grampp et al.
1998; Yochum and Barry 1997).
The potential role of limb malalignment and bone marrow edema was described by Felson et al. (2003).
Medial bone marrow lesions can be seen in athletes with varus limb, whereas lateral lesions are associ- ated with valgus limbs.
The importance of alignment is experimentally demonstrated by Libicher et al. (2005) in an in vivo MRI demonstration of the Pond-Nuki animal model for the evaluation of osteoarthritis. In this experi- mental study, 24 beagle dogs underwent transsection of the anterior cruciate ligament of the left leg (modi- fi ed Pond-Nuki model). The fi rst sign on MRI was the appearance of subchondral bone marrow edema at the posteromedial aspect of the tibia followed by pro- gressive cartilage degeneration, meniscus degenera- tion and osteophytosis.
6.3.3
Lesions of Unknown Pathogenesis
Bone marrow edema syndromes without any his- tory of trauma are increasingly recognized on MRI ( Mandalia et al. 2005).
Distinction between bone bruising and marrow edema syndromes is primarily based on the clinical history of the patient.
6.3.3.1
Bone Marrow Edema Syndrome
Transient bone marrow edema syndrome (BMES) is an unusual but distinct selfl imiting syndrome located at the weight bearing joints of the lower limbs (Toms et al. 2005). It usually affects middle-aged men and women in the last trimester of pregnancy, but association with sports activities has been reported ( Miltner et al. 2003).
Fig. 6.8. Impaction type bone marrow edema, associated with lateral patellar dislocation in a soccer player. An axial fat sup- pressed FSE T2-weighted image of the right knee demonstrates BME involving the medial patellar facet and the anterior aspect of the lateral femoral condyle. Associated distraction at the medial patellar retinaculum will result in thickening and extensive hyperintensity due to partial disruption
BMES usually affects only one bone, predominantly the proximal femur. The tarsal bones and the knee joint are involved less frequently (Radke et al. 2001).
Three distinct clinical phases have been described (Schapira 1992). In the fi rst phase, pain is rapidly aggravated, with functional disability lasting approx- imately one month. The second phase, lasting one or two months, the pain reaches a plateau phase. The third phase is characterized by regression of symp- toms. This period lasts approximately four months.
Imaging features consist of BME without associ- ated fi ndings on MRI (Hayes et al. 1993).
In the second phase of the disease, osteopenia may be present on the plain radiographs, whereas the third phase is characterized by reconstitution of bone density (Fig. 6.9).
Regional migratory Bone Marrow Edema Syndrome is a special form of BMES, characterized by migration between the weight-bearing joints. The lower limbs are most frequently involved (Hofmann 1999).
6.3.3.2
Bone Marrow Edema in Long Distance Runners Bone marrow edema can be seen in recreational athletes one to eight weeks after sports running ( Krampla et al. 2001; Trappeniers et al. 2003). The
affected bones included the knee and the tarsal and metatarsal bones. STIR or T2-WI with spectral fat suppression are most sensitive to detect these edema patterns.
6.3.3.3
Subchondral Insuffi ciency Fracture
The concept of subchondral insuffi ciency fracture and its relationship with spontaneous osteonecrosis (SONK) and rapidly destructive osteoarthritis will be discussed briefl y in Chap. 7 with regard to “overuse trauma and stress fractures”.
6.4
Histopathological Correlation
A variety of histologic studies of patients with BME have been described with different results. Some studies revealed necrosis of cellular elements in the subchondral bone, trabecular microfractures and hemorrhage and edema (Johnson et al. 1998;
Rangger et al. 1998; Ryu et al. 2000), whereas others demonstrated only edema with displacement of cel-
Fig. 6.9a,b. Bone Marrow Edema Syndrome of the right foot two months after onset of symptoms at the foot. a Sagittal fat sup- pressed FSE T2-weighted image showing multifocal BME at the tarsal bones. b Plain radiograph demonstrating the presence of patchy osteopenia of the foot
a b
lular elements, but absence of necrosis (Escalas and Curell 1994).
Review of the different histologic studies suggests that differing degrees and severity of injury may determine the differing histological patterns. Rela- tively less severe trauma causes marrow edema with- out obvious injury to the cellular element, whereas with increasing severity of trauma microfractures and hemorrhage are seen within the trabecular bone (Mandalia et al. 2005).
6.5
Clinical Signifi cance
The clinical signifi cance of bone marrow edema has been an issue of discussion even since the fi rst reports on bone bruise.
It is very diffi cult to identify clinical signs and symptoms directly attributable to the underlying bone bruising, because there are usually associated soft tissue changes (Mandalia et al. 2005).
In a prospective study of 95 patients with inversion injuries of the ankle and no fracture on plain radio- graphs, Alanen et al. (1998) found an incidence of bone bruises of 27%. Most of the bruises were located in the talus, typically in the medial part.
The authors found no statistical difference in the time to return to work, limitation in walking or phys- ical activity and clinical outcome at three months in two groups with and without BME. These fi ndings were in line with a previous study by Zanetti et al.
(1997).
Vincken et al. (2005) evaluated the clinical conse- quences of bone bruise on MRI around the knee in 664 consecutive patients with subacute knee complaints.
They evaluated the relation between bone bruise and (peri-)articular derangement and the impact of bone bruise at the time of MRI and six months thereafter.
Bone bruises were diagnosed in 18.7% of patients.
They concluded that bone bruise is no predictor for the presence of intra-articular pathology. Indeed, prevalence of bone bruise was not signifi cantly dif- ferent between patients with (21%) and those with- out (16%) intra-articular pathology. Bone bruise was particularly associated with tears in anterior cruciate ligaments, collateral ligaments and lateral meniscus, whereas the medial meniscus tears (although rep- resenting the most common knee lesion) were not associated with bone bruise.
On the other hand, patients presenting with bone bruise at the time of MRI had a signifi cant higher level of symptoms, functional defi cit and decrease in activity.
In particular, the presence of bone bruise and MCL tear has the most impact on function and symptoms at the time of MRI.
However, bone bruise did not have any effect on function, symptoms and activity at six months.
Future long-term prospective studies are required to answer the question related to the clinical signifi - cance of BME.
6.6
Natural Evolution
6.6.1
Follow-up of Acute Traumatic Bone Marrow Edema
The reported time for the resolution of bone bruis- ing is variable, ranging from as early as three weeks to two years (Mandalia et al. 2005; Roemer and Bohndorf 2002). This variability may be attrib- uted to several factors, such as the severity of injury, extent of bone bruising and other associated internal knee derangement. Future large prospective studies are required to validate those factors affecting the radiological evolution of bone bruising (Mandalia et al. 2005).
Two patterns of bruise resolution have been described by Davies et al. (2004). The centripetal pattern is the most frequent (Fig. 6.10.), whilst other lesions (mostly types IIb and III) tend to resolve towards the joint margin (see also Chap. 28). The latter generally resolve more slowly and probably require longer rehabilitation because of higher risk of premature osteo-arthritis.
The natural history of bruises is not well known as well as whether they predispose to premature osteo- arthritis.
Many studies have shown that bone bruising may have a deleterious effect on the overlying articular car- tilage, although this concept is not generally accepted (Mandalia et al. 2005). The pathophysiological mechanisms by which the cartilage can undergo this degenerative process may be multifactorial. The ini- tial blunt trauma might exceed a supraphysiological threshold and lead to progressive chondral damage
(Mankin 1982). Additionally, the osseous lesion might heal into a stiffer construction than the previ- ous normal bone. The decreased compliance might then generate greater loads in the articular cartilage, leading to a progressive cartilage degeneration.
6.6.2
Follow-up of Chronic Traumatic Lesions
This item will be described more in detail in Chap. 28 on “Monitoring and Natural History of Fractures and Microfractures”.
6.6.3
Follow-up of BMES
In BMES, the mean interval from the onset of symp- toms until complete clinical resolution ranges from 4 to 24 months, with an average of 6 months. All patients with BMES recover completely without intervention. Therefore, the term transient BMES can be used. Recovery, however, can be speeded up with vasodilatators (Aigner et al. 2002).
6.7
Conclusion
BME is a relatively recently recognized entity. MRI has proved to be the most powerful tool to assess BME, as conventional imaging techniques are insen- sitive for detection of trabecular injuries.
The pathogenesis of BME is variable and may be due to acute or chronic trauma or even causes with- out any history of obvious trauma.
Distinction between traumatic and non-traumatic bone marrow edema in sports injuries is primarily based on a clinical history of trauma, as imaging fea- tures are mostly indistinguishable.
In traumatic cases, the pattern of bone marrow edema, however, may reveal the mechanism of under- lying trauma and is often a secondary sign for detect- ing associated abnormalities.
The clinical signifi cance of BME is still a matter of debate, and long-term follow-up studies are required for further evaluation of this item.
Fig. 6.10a,b. Resolution pattern of BME. Coronal fat suppressed FSE T2 weighted image of the right knee at the moment of a direct trauma at the knee (a) and after three months follow-up (b). a Extensive impaction BME at the proximal tibia.
b There is centripetal resolution of BME, with some residual BME at the center of the original lesion
a b
Things to Remember
1. MRI is the imaging modality of choice to detect bone marrow lesions in sports injuries.
Fat-suppressed T2-weighted images or (S)TIR sequences are the most sensitive-ones.
2. Mostly BME in itself is benign/self lim- ited. Longer follow-up studies are needed to determine the clinical importance of the osteochondral sequelae and to evaluate the possible evolution towards premature degen- eration. Isolated bruise can be the cause of pain.
3. Moreover, a systematic analysis of the BME- pattern often reveals a specifi c underlying trauma-mechanism. This can help to detect the associated soft tissue lesions, which are often less conspicuous.
4. Residual indications for conventional radiog- raphy (and/or CT) are (subtle) avulsion frac- tures and some stress fractures.
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