B

A

ktfi©

K

ia[ef

1h

gafe

cfhcrob

0d

European Journal of Radiology 67 (2008) 68–77

one marrow edema of the femoral head and transient osteoporosis of the hip

Bruno C. Vande Berg ∗, Frederic E. Lecouvet, Sophie Koutaissoff,Paolo Simoni, Jacques Malghem

Department of Radiology and Medical Imaging, Universite Catholique de Louvain, University Hospital St Luc,10 Avenue Hippocrate 1200, Brussels, Belgium

Received 17 January 2008; received in revised form 17 January 2008; accepted 18 January 2008

bstract

The current article of this issue aims at defining the generic term of bone marrow edema of the femoral head as seen at MR imaging. It must be

ept in mind that this syndrome should be regarded, not as a specific diagnosis, but rather as a sign of an ongoing abnormal process that involveshe femoral head and/or the hip joint. We aim at emphasizing the role of the radiologists in making a specific diagnosis, starting from a non-specificnding on T1-weighted images and by focusing on ancillary findings on T2-weighted SE or fat-saturated proton-density weighted MR images.2008 Elsevier Ireland Ltd. All rights reserved.

toaoomaimSfaspresent. The adjacent soft tissues are generally normal.

Epidemiological data on the bone marrow edema syndromeare sparse. In a consecutive series of 60 patients with a transientbone marrow edema syndrome of the femoral head, there were

Table 1Morphological criteria of the bone marrow edema of the femoral head on T1-

eywords: Bone marrow; Edema; Femoral head; Osteoporosis; Osteonecrosis

The phrase “bone marrow edema”, is routinely used in clin-cal practice to indicate the presence of a pattern of marrowlteration that is common to numerous bone and joint disorders1,2]. The current article focuses on the definition and differ-ntial diagnosis of the bone marrow edema syndrome of theemoral head.

. The bone marrow edema syndrome of the femoralead

The “bone marrow edema syndrome” of the femoral head is aeneric term used to refer to a lesion pattern seen at MR imagingnd characterized by altered marrow signal intensity within theemoral head suggestive of medullary infiltration by interstitialdema [3–5] (Fig. 1).

Four morphologic criteria on T1-weighted SE images indi-ate the presence of the bone marrow edema syndrome of theemoral head (Table 1). First, the lesion must involve the femoralead. It generally involves the upper pole and reaches the sub-

hondral bone [5,6]. It may extend into the femoral neck and,arely, subtle marrow changes also involve the acetabulum. Sec-nd, the lesion lacks definite margins and the transition zoneetween the lesion and the adjacent marrow is large [4,7]. Third,

∗ Corresponding author. Tel.: +32 2 764 29 52; fax: +32 2 770 74 55.E-mail address: bruno.vandeberg@uclouvain.be (B.C. Vande Berg).

w

T

MO

S

720-048X/$ – see front matter © 2008 Elsevier Ireland Ltd. All rights reserved.oi:10.1016/j.ejrad.2008.01.061

he lesion signal is homogeneous, without obvious focal roundr lobulated changes and without residual intralesional fattyreas. Finally, the lesion signal intensity is moderately reducedn T1-weighted SE images. All these features must be seenn T1-weighted images. The lesion’s signal intensity is inter-ediate to high on T2-weighted SE images and high on STIR

nd fat-saturated intermediate- or T2-weighted images. Afterntravenous contrast injection, homogeneous and moderate to

arked signal intensity enhancement is seen on T1-weightedE images [5,8]. At close inspection of these sequences, subtleocal changes can occasionally be detected in the subchondralrea. These additional changes may represent clues to a morepecific diagnosis (Table 2). A moderate joint effusion is usually

eighted SE MR images

opography At least femoral head (subchondral area), also infemoral neck

argins Ill-defined margins, no peripheral rimverall appearance Homogeneous, no high or low signal foci in the

lesionignal intensity Moderately reduced

B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77 69

Fig. 1. Insufficiency stress fracture in a 43-year-old man with diffuse osteopenia. (a) The coronal T1-weighted SE image demonstrates abnormal femoral head signalintensity that predominates in the subchondral region and also involves the femoral neck. The lesion is ill-delimited. Another lesion with sharp margins and morepronounced and homogeneous decrease in signal intensity involves the femoral neck. The latter lesion is unlikely to represent marrow edema. (b) The correspondingT2-weighted SE image shows intermediate signal intensity in the femoral head and moderate joint swelling. (c) The sagittal T1-weighted SE image of the femoralhead demonstrates the moderate decrease in signal intensity, the lack of obvious margins and the predominance of the marrow alteration in the subchondral area. (d)The sagittal T2-weighted SE image demonstrates the presence of a small band of low signal intensity that runs parallel to the subchondral bone plate and is locatedat a few millimeters from it. This band is likely to correspond to an impaction fracture of the trabecular bone. The femoral head lesion completely and spontaneouslydisappeared at MR follow-up, whereas the femoral neck lesion remained unchanged.

Table 2MR features observed in the bone marrow edema syndrome that may help in diagnosis and prognosis

Additional MR features Diagnosis Prognosis

Cartilage loss Osteoarthritis (or advanced osteonecrosis) IrreversibleFrank femoral head deformity Osteonecrosis (rarely osteoarthritis) IrreversibleSubchondral cleft fracture a Osteonecrosis (rarely osteoarthritis) IrreversibleCrescent-shaped low signal intensity subchondral area Osteonecrosis, osteoarthritis, insufficiency fracture Variableb

Subchondral impaction fracturec Insufficiency fracture or transient osteoporosis ReversibleNo other change Transient osteoporosis or idiopathic bone marrow edema or stress fracture Reversible

a A subchondral cleft fracture appears as a subchondral line of high signal intensity on T2-weighted SE images that is parallel to the subchondral bone plate.b Determination of the thickness of this area can contribute to better differentiate irreversible from reversible lesions.c A subchondral impaction fracture appears as a subchondral line of low signal intensity on T2-weighted SE images that is parallel to the subchondral bone plate.

70 B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77

Fig. 2. Transient osteoporosis. (a) Radiograph of the right hip shows severe osteoporosis with vanishing femoral head contour and normal joint space. (b) CoronalT1-weighted SE image of the pelvis shows moderate decrease in signal intensity with ill-defined margins in the femoral head suggestive of the bone marrow edemasyndrome. (c) Sagittal T1-weighted SE image shows that the abnormal signal predominates in the subarticular area. The acetabular bone is normal. (d) The abnormalmarrow demonstrates high signal intensity on the corresponding T2-weighted SE image. (e) The sagittal T1-weighted SE image obtained several months laterdemonstrates a return to a normal signal pattern.

B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77 71

Table 3MR features useful for the differential diagnosis between impaction fractures and reactive interface of infarcts

Impaction fracture Rim of infarct

Topography Near bone plate At distance from bone plateOrientation Parallel to bone plate variableMorphology Thin, short Large, serpiginousTE een thM dens

3ywim

raalcdNou

t[

rsatrrco

Fea

2-weighted images Low signalnhanced T1-weighted Low signal, better sost prominent on Fat-saturated proton

7 male and 23 female patients with a mean age of 49 and 48ears, respectively [9]. In this series, about half of the lesionsere observed in association with various medical conditions

ncluding pregnancy, glucocorticoid therapy, alcohol abuse, andetabolic bone diseases.At histology, the most characteristic feature of bone mar-

ow edema syndrome of the femoral head is focal area of thinnd disconnected bone trabeculae covered by osteoid seams andctive osteoblasts with formation of irregular woven bone (cal-us) [10]. The surrounding bone marrow tissue shows edematoushanges and mild fibrosis, frequently associated with fat cell

estruction, vascular congestion and/or interstitial hemorrhage.o osteonecrotic region is observed in either the bone trabeculaer the bone marrow tissue. In addition to increased osteoid vol-me, a decreased maximal hydroxyl apatite content and a shift

o[sb

ig. 3. Migratory bone marrow edema syndrome. (a) Coronal T1-weighted SE imagdema syndrome of the left femoral head. (b) Two months later, a follow-up coronalfter the initial study, right hip pain appeared and a coronal T1-weighted SE image of

Double-line signan on SE T1 Less well seen than on SE T1ity T1-weighted SE

o undermineralized bone can be found by mineral densitometry11].

The pathophysiology of the bone marrow edema syndromeemains unknown. Links with ischemia, fractures and reflexympathetic dystrophy syndrome have been suggested. Fromclinical point of view, it is important to keep in mind that

he bone marrow edema syndrome is non-specific and probablyesults from different causes [12]. Subsequently, the bone mar-ow edema syndrome of the femoral head shows a variable timeourse, depending on the underlying causes that include transientsteoporosis of the hip [3,13], idiopathic bone marrow edema

f the hip [4,6], traumatic or stress fracture of the femoral head14,15], hip osteoarthritis [16–18] and femoral head osteonecro-is [19,20]. The distinction between these conditions is crucialecause of their different outcomes [6]. Transient osteoporo-

e of the pelvis of a 67-year-old man with left hip pain shows the bone marrowT1-weighted SE image shows disappearance of the lesion. (c) Eleven monthsthe pelvis showed the bone marrow edema syndrome in the right femoral head.

7 Journ

sse[sf

2

cra(l

to

teopmgwe

Flis

2 B.C. Vande Berg et al. / European

is and idiopathic bone marrow edema syndrome are generallypontaneously self-limited. Insufficiency stress fracture mayither completely resolve or progress toward epiphyseal collapse21]. Finally, hip osteoarthritis and femoral head osteonecro-is are not spontaneously reversible and can lead to jointailure.

. Transient osteoporosis of the hip

Transient osteoporosis of the hip is an uncommon clini-al entity characterized by the spontaneous appearance and

esolution over time of hip pain and the associated delayedppearance of marked osteoporosis of the femoral head [22,23]Fig. 2). MR imaging does not enable recognition of this pecu-iar entity but its widespread use has facilitated the detection of

bgds

ig. 4. Femoral head osteonecrosis. (a) A coronal T1-weighted SE image shows theesion is very low. (b) A sagittal fat-saturated intermediate-weighted images shows thn the antero-superior aspect of the femoral head, indicative of necrosis. Note that thhows femoral head osteonecrosis with marked epiphyseal collapse.

al of Radiology 67 (2008) 68–77

he bone marrow edema syndrome that is observed in transientsteoporosis.

This condition generally involves adult male patients with aypical time course of clinical and radiographic changes. Unilat-ral hip pain begins spontaneously, may be rapid or gradual innset and is aggravated by weight-bearing. After a plateau phase,ain progressively decreases until complete regression by 6–12onths after the onset, without residual sequelae. Initial radio-

raphs are normal, but marked osteoporosis of the femoral headith preserved joint space is seen on radiographs obtained sev-

ral weeks after the onset of symptoms. The bone resorption can

e so intense that the subchondral bone plate becomes indistin-uishable on conventional radiographs. Follow-up radiographsemonstrate a return to a normal appearance. Radionuclidetudies with bone-seeking agents reveal abnormal accumula-

bone marrow edema syndrome in the femoral head. Note that the signal of thee presence of a subchondral crescent-shaped low signal intensity area (arrow)e cartilage appears normal. (c) Follow-up radiograph obtained 3 months later

Journ

tmoestm[

fpo

as

3

ao

Fa(ms

B.C. Vande Berg et al. / European

ion of isotope in the femoral head. At MR imaging, the bonearrow edema syndrome is observed [3,5,13]. The severity

f osteopenia does not correlate with the extent of marrowdema [24]. Discrete additional changes can be seen in theubchondral area, including low signal intensity lines and sub-le depression of the subchondral bone plate in some or the

ajority of cases of transient osteoporosis of the femoral head25].

In general, the diagnosis of transient osteoporosis of theemoral head remains presumptive, until demonstration of com-lete resolution of clinical and radiological changes. Transientsteoporosis does not recur in the same joint but may involve

sity

ig. 5. Typical femoral head osteonecrosis and marrow edema in a 23-year-old wombnormal signal in the left femoral head and neck. (b) On a coronal T1-weighted iarrow) separates the proximal lesion from the infiltrated marrow. (c) On the corresparrow shows intermediate signal intensity. This lesion pattern is indicative of femo

hows collapse of the left femoral head with low signal in the lesion and a normal fem

al of Radiology 67 (2008) 68–77 73

nother lower limb epiphysis, a situation called migratory tran-ient osteoporosis (Fig. 3).

. Insufficiency or stress fractures of the femoral head

Fractures of the trabecular bone of the femoral head aren ubiquitous finding observed in resected specimens forsteoarthritis, arthritis, avascular necrosis, transient osteoporo-

is and rapidly destructive osteoarthritis [21]. The concept ofsolated trabecular fatigue (normal stress – weakened bone) ofhe femoral head has progressively emerged during the last 15ears, thanks to the use of MR imaging [14,15,26–30]. Insuffi-

an with steroid therapy. (a) Coronal T1-weighted SE image of both hips showsmage, marrow edema predominates in the femoral neck. A rim of low signalonding T2-weighted SE image, the lesion is barely visible. The femoral neckral head osteonecrosis. (d) Three months later, a coronal T1-weighted imageoral neck marrow.

7 Journ

cbadafr

taSfopnrasT

pamblbasidl

4

Foir

4 B.C. Vande Berg et al. / European

iency fractures of the femoral head is one of the cause of theone marrow edema syndrome of the femoral head (Fig. 1). Inddition to bone marrow edema, two morphological changes areiagnostic clues for insufficiency fractures, although they canlso be observed in transient osteoporosis [24]. In insufficiencyractures, marked and focal osteopenia is generally lacking onadiographs.

First, impaction fractures of the trabecular bone appear ashin low signal intensity bands or lines or more globular speckledreas of low signal intensity on the T2- or enhanced T1-weightedE images. They should not be confused with the reactive inter-ace or rim that surrounds marrow infarcts (Table 3). The planef impaction fractures runs parallel to the subchondral bonelate at a small distance from the articular surface and doesot delineate a large marrow area [31]. It is surrounded by mar-

ow edema on both sides (with no residual fat in the subchondralrea) and it does not show the double-line sign on T2-weightedpin-echo images. These lines are generally more prominent on2-weighted than on T1-weighted sequences.

ohfi

ig. 6. Osteoarthritis and bone marrow edema syndrome in a 74-year-old woman. (asteophytes. (b) Coronal T1-weighted SE image shows abnormal femoral head mantermediate-weighted image shows narrowing of the anterior joint space and abrasielated to the development of cartilage abrasion. Total hip replacement was performe

al of Radiology 67 (2008) 68–77

Second, subtle focal deformity of the subchondral bonelate is occasionally visible in the antero-superior or lateralspects of the femoral head, just below the acetabular roofargin. This probably represents discrete impaction of the

one plate separating the articular cartilage from the under-ying bony trabeculae. These depressions of the subchondralone plate remain limited and are not as abrupt or as markeds the overt fractures that occur in epiphyseal osteonecro-is. They can be better seen on intermediate-weighted SEmages or contrast-enhanced T1-weighted SE images probablyue to a high signal contrast between marrow and carti-age.

. Femoral head osteonecrosis

Extensive marrow edema can be observed in femoral headsteonecrosis in at least three different situations. First, femoralead osteonecrosis can develop as an isolated predominantnding, mainly in elderly patients, in a manner reminiscent to

) Radiograph of the pelvis shows joint space narrowing of the left hip withoutrrow, joint swelling but normal acetabular marrow. (c) Sagittal fat-saturatedon of the cartilage. Marrow edema of the femoral head marrow is most likelyd a few months later.

Journ

tlhkaStrosstTt[fsai

aocipsoi9

os

pmpclesnwlrtieso

rhtr

TFa

B.C. Vande Berg et al. / European

hat of spontaneous osteonecrosis of the knee (Fig. 4). Thisesion pattern represents about 10% of symptomatic femoralead osteonecrosis [5,7,19,32]. It is observed in patients withoutnown risk factors for avascular necrosis and is usually notssociated with marrow infarcts in other bones. On T1-weightedE images, there is no residual fat within the necrotic lesion and

here is no interface at its periphery. In this case of the bone mar-ow edema syndrome, careful analysis of the subchondral arean T2- or fat-saturated intermediate-weighted images usuallyhows additional features suggestive of epiphyseal osteonecro-is. First, a crescent-shaped low signal intensity area is seen inhe subchondral area, delineated at its lower aspect by edema.his low signal intensity area is reminiscent to that of necrotic

issue observed in classic forms of epiphyseal osteonecrosis33–35] and in spontaneous osteonecrosis of the knee. Second,emoral head deformity can be observed and indicates epiphy-eal collapse compatible with femoral head osteonecrosis. Thesedditional changes are barely visible on the T1-weighted SEmages.

Unfortunately, these two changes are not specific and canlso be observed in insufficiency stress fractures and transientsteoporosis. To some extent, determination of their importanceontributes to differentiate irreversible (osteonecrosis, somensufficiency fractures) from reversible lesions (transient osteo-orosis, some insufficiency fractures). A low signal intensity

ubchondral area with a thickness equal or superior to 4 mm (inther words, thicker than the articular space) on T2-weightedmages suggests an irreversible lesion with a specificity of about2% [9]. Marked femoral head contour deformity also indicates

5

t

able 4low chart for systematic analysis of the bone marrow edema syndrome of the femond most likely diagnoses

al of Radiology 67 (2008) 68–77 75

steonecrosis but this feature can be difficult to assess on crossectional images.

Second, in systemic osteonecrosis (the condition observed inatients with multiple marrow infarcts associated with inflam-atory diseases, alcohol abuse or steroid treatment) and in

ost-traumatic osteonecrosis, extensive head and neck edemaan occur [36–40] (Fig. 5). In this condition, a focal ischemicesion involves the upper pole of the femoral head, and marrowdema occurs more distally, in the femoral head and neck andpares the proximal lesion. Therefore, this lesion pattern doesot correspond to a true bone marrow edema syndrome. The T1-eighted SE image better displays the ischemic femoral head

esion because this lesion contains residual marrow fat and is sur-ounded by a low signal intensity rim. Many authors agree onhe hypothesis that marrow edema distal to a subchondral infarcts an indirect sign of epiphyseal fracture [40–43], although oth-rs believe that edema represent progressive ischemia. Othertudies also indicated that this typical pattern of femoral headsteonecrosis is not preceded by marrow edema [44,45].

Finally, femoral head osteonecrosis can also show bone mar-ow edema in patients with haematological conditions or reactiveaematopoietic marrow hyperplasia [46–49]. In this situation,he entire marrow is abnormal and the lesion develops in aed-marrow equivalent area and not in yellow marrow.

. Osteoarthritis

Osteoarthritis of the hip can generally be recognized byhe presence of subchondral cysts, subchondral bone sclerosis

ral head femoral head indicating sequences, possible focal lesions, prognosis

7 Journ

aTftpt[omtaaoodiHef[

6f

otn

tof

dS(ritiiui

taiiciptarlfa

R

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

6 B.C. Vande Berg et al. / European

nd, at close inspection, focal or extensive cartilage changes.hese changes generally involve both the acetabulum and the

emoral head. However, in some unusual cases, hip osteoarthri-is shows the bone marrow edema syndrome (Fig. 6). This lesionattern has been recognized in rapidly progressive osteoarthri-is, a condition which can rapidly lead to joint destruction16–18]. In rapidly progressive osteoarthritis, a combinationf bone and marrow changes can be seen, including defor-ity of the subchondral bone plate, impaction fractures of

he trabecular bone and extensive marrow infiltration. Gener-lly, marginal osteophytes are absent. The presence of cartilagebrasion is the diagnostic clue, but it may be difficult to rec-gnize. This lesion pattern is very similar to that of epiphysealsteonecrosis. In osteonecrosis, cartilage abrasion parallels theegree of epiphyseal deformity, although massive femoral headnfarction can rapidly cause proximal femur destruction [50].ypothetically, cartilage lesion could develop early in the dis-

ase course in rapidly evolving osteoarthritis and could beollowed by the development of bone fracture and marrow edema21,51].

. Recommended analysis pattern of MR images ofemoral head bone marrow edema

A careful and systematic analysis of the MR images is rec-mmended when facing the bone marrow edema syndrome ofhe femoral head, given the variable outcomes observed in theumerous conditions showing this syndrome [12] (Table 4).

First, analysis of the T1-weighted SE images is mandatoryo differentiate a true “bone marrow edema syndrome” fromther lesions in which marrow edema can also be a predominanteature like tumors, infection, cysts and systemic osteonecrosis.

Second, after confirmation of the bone marrow edema syn-rome on T1-weighted SE images, high-resolution T2-weightedE sequences are useful to assess (a) the articular cartilage,b) the subchondral bone plate and (c) the subchondral mar-ow. Several rules are useful: (a) if the articular cartilages abnormal, the lesion is clinically irreversible (osteoarthri-is or osteonecrosis); (b) if the subchondral bone plate isnterrupted and the epiphysis lacks sphericity, the lesion isrreversible; (c) if a fluid-like signal intensity plane is visiblenderneath the epiphyseal contour (cleft fracture), the lesion isrreversible.

Finally, after exclusion of a cartilage lesion and obvious frac-ure of the subchondral bone plate, detection and quantitativessessment of possible focal subchondral changes (low signalntensity subchondral area on T2- or enhanced T1-weighted SEmages), may yield information relevant to the spontaneous out-ome of these lesions. The lack of any additional focal changesn the subchondral edematous marrow area indicates a favorablerognosis, i.e. spontaneous resolution of the lesions and symp-oms. The presence of a crescent-shaped low signal intensityrea in the subchondral region with a thickness equal or supe-

ior to 4 mm on T2-weighted images suggests an irreversibleesion. In some situations, the prognosis remains uncertain andollow-up MR studies obtained 3 months later represent a validlternative to further evaluate the femoral head lesion.

[

[

al of Radiology 67 (2008) 68–77

eferences

[1] Vogler JBI, Murphy WA. Bone marrow imaging. Radiology 1988;168(3):679–93.

[2] Vande Berg BC, Malghem J, Lecouvet FE, Maldague BE. Classificationand detection of bone marrow lesions with magnetic resonance imaging.Skelet Radiol 1998;27:529–45.

[3] Wilson AJ, Murphy WA, Hardy DC, Totty WG. Transient osteoporosis:transient bone marrow edema? Radiology 1988;167:757–60.

[4] Hayes CW, Conway WF, Daniel WW. MR imaging of bone marrow edemapattern: transient osteoporosis, transient bone marrow edema syndrome, orosteonecrosis. Radiographics 1993;13(5):1001–11.

[5] Vande Berg BC, Malghem J, Labaisse MA, Noel HM, Maldague BE. MRimaging of avascular necrosis and transient marrow edema of the femoralhead. Radiographics 1993;13(3):501–20.

[6] Conway WF, Totty WG, McEnery KW. CT and MR imaging of the hip.Radiology 1996;198(2):297–307.

[7] Mitchell DG, Rao VM, Dalinka MK, et al. Femoral head avascular necrosis:correlation of MR imaging, radiographic staging, radionuclide imaging,and clinical findings. Radiology 1987;162(3):709–15.

[8] Koo KH. Increased perfusion of the femoral head in transient bone marrowedema syndrome. Clin Orthop Relat Res 2002;402:171–5.

[9] Vande Berg BC, Malghem J, Lecouvet FE, Jamart J, Maldague B. Idiopathicbone marrow edema lesions of the femoral head: predictive value of MRimaging findings. Radiology 1999;212:527–35.

10] Yamamoto T, Kubo T, Hirasawa Y, Noguchi Y, Iwamoto Y, Sueishi K. Aclinicopathologic study of transient osteoporosis of the hip. Skelet Radiol1999;28(11):621–7.

11] Plenk H, Hofmann S, Eschberger J, et al. Histomorphology and bone mor-phometry of the bone marrow edema syndrome of the hip. Clin OrthopRelat Res 1997;334:73–84.

12] Vande Berg BC, Malghem J, Lecouvet FE, Maldague B. Magnetic res-onance imaging and differential diagnosis of epiphyseal osteonecrosis.Semin Musculoskelet Radiol 2001;5(1):57–67.

13] Bloem JL. Transient osteoporosis of the hip: MR imaging. Radiology1988;167(3):753–5.

14] Rafii M, Mitnick H, Klug J, Firooznia H. Insufficiency fracture ofthe femoral head: MR imaging in three patients. Am J Roentgenol1997;168:159–63.

15] Vande Berg BC, Malghem J, Goffin EJ, Duprez TP, Maldague BE. Transientepiphyseal lesions in renal transplant recipients: presumed insufficiencystress fractures. Radiology 1994;191(2):403–7.

16] Boutry N, Paul C, Leroy X, Fredoux D, Migaud H, Cotten A. Rapidlydestructive osteoarthritis of the hip: MR imaging findings. AJR Am JRoentgenol 2002;179(3):657–63.

17] Sugano N, Ohzono K, Nishii T, et al. Early MRI findings of rapidly destruc-tive coxopathy. Magn Reson 2001;19(1):47–50.

18] Watanabe W, Itoi E, Yamada S. Early MRI findings of rapidly destructivecoxarthrosis. Skelet Radiol 2002;31(1):35–8.

19] Turner DA, Templeton AC, Selzer PM, Rosenberg AG, Petasnick JP.Femoral capital osteonecrosis: MR finding of diffuse marrow abnormalitieswithout focal lesions. Radiology 1989;171(1):135–40 [see comments].

20] Mitchell DG, Kressel HY. MR imaging of early avascular necrosis. Radi-ology 1988;169(1):281–2 [letter].

21] Davies M, Cassar-Pucillino V, Darby A. Subchondral insufficiency frac-tures of the femoral head. Eur Radiol 2004;14(2):201–7.

22] Curtis Jr PH, Kincaid WE. Transitory demineralization of the hip inpregnancy: a report of three cases. J Bone Joint Surg (Am) 1959;41:1327–33.

23] Lequesne M. Transient osteoporosis of the hip. A nontraumatic variety ofSudeck’s atrophy. Ann Rheum Dis 1968;27:463–71.

24] Malizos KN, Zibis A, Dailiana Z, Hantes M, Karahalios T, Karantanas A.MR imaging findings in transient osteoporosis of the hip. Eur J Radiol

2004;50:238–44.

25] Miyanishi K, Yamamoto T, Nakashima Y, et al. Subchondral changes intransient osteoporosis of the hip. Skelet Radiol 2001;30(5):255–61.

26] Visuri T. Stress osteopathy of the femoral head—10 military recruits fol-lowed for 5–11 years. Acta Orthop Scand 1997;68(2):138–41.

Journ

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

B.C. Vande Berg et al. / European

27] Prues-Latour V, Bonvin JC, Fritschy D. Nine cases of osteonecrosis inelderly patients following arthroscopic meniscectomy. Knee Surg SportsTraumatol Arthrosc 1998;6(3):142–7.

28] Yamamoto T, Bullough PG. Subchondral insufficiency fracture of thefemoral head: a differential diagnosis in acute onset of coxarthrosis in theelderly. Arthritis Rheum 1999;42(12):2719–23.

29] Yamamoto T, Schneider R, Bullough PG. Insufficiency subchon-dral fracture of the femoral head. Am J Surg Pathol 2000;24(3):464–8.

30] Yamamoto T, Bullough PG. Subchondral insufficiency fracture of thefemoral head and medial femoral condyle. Skelet Radiol 2000;29(1):40–4.

31] Arndt WF, Truax AL, Barnett FM, Simmons GE, Brown DC. MRdiagnosis of bone contusions of the knee: comparison of coronal T2-weighted fast spin-echo with fat saturation and fast spin-echo STIR imageswith conventional STIR images. AJR Am J Roentgenol 1996;166(1):119–24.

32] Thickman D, Axel L, Kressel HY, et al. Magnetic resonance imagingof avascular necrosis of the femoral head. Skelet Radiol 1986;15(2):133–40.

33] Bjorkengren AG, AlRowaih A, Lindstrand A, Wingstrand H, ThorngrenKG, Pettersson H. Spontaneous osteonecrosis of the knee: value of MRimaging in determining prognosis. AJR Am J Roentgenol 1990;154(2):331–6.

34] Vande Berg BC, Malghem J, Labaisse MA, Noel H, Maldague B. Avascularnecrosis of the hip: comparison of contrast-enhanced and nonenhanced MRimaging with histologic correlation. Radiology 1992;182(2):445–50 [workin progress].

35] Garagiola DM, Clark SA, Colyer RA, Braunstein EM. Case report 536:chronic tophaceous gout in a 17-year-old male. Skelet Radiol 1989;18(5):377–9.

36] Lang P, Jergesen HE, Moseley ME, Block JE, Chafetz NI, GenantHK. Avascular necrosis of the femoral head: high-field-strengthMR imaging with histologic correlation. Radiology 1988;169(2):517–24.

37] Jergesen HE, Lang P, Moseley M, Genant HK. Histologic correlation in

magnetic resonance imaging of femoral head osteonecrosis. Clin Orthop1990;253:150–63.

38] Hauzeur JP, Pasteels JL, Schoutens A, et al. The diagnostic value of mag-netic resonance imaging in non-traumatic osteonecrosis of the femoralhead. J Bone Joint Surg Am 1989;71(5):641–9.

[

al of Radiology 67 (2008) 68–77 77

39] Sakai T, Sugano N, Nishii T, Haragushi K, Ochi T, Ohzono K. MR findingsof necrotic lesions and the extralesional area of osteonecrosis of the femoralhead. Skelet Radiol 2000;29:133–41.

40] Koo KH, Ahn IO, Song HR, et al. Bone marrow edema and associated painin early stage osteonecrosis of the femoral head: prospective study withserial MR images. Radiology 1999;213:715–22.

41] Iida S, Harada Y, Shimizu K, et al. Correlation between bone marrow edemaand collapse of the femoral head in steroid-induced osteonecrosis. AJR AmJ Roentgenol 2000;174(3):735–43.

42] Huang GS, Chan WP, Chang YC, Chang CY, Chen CY, Yu JS. MR imagingof bone marrow edema and joint effusion in patients with osteonecro-sis of the femoral head: relationship to pain. AJR Am J Roentgenol2003;181(2):545–9.

43] Stevens K, Tao C, Lee SU, et al. Subchondral fractures in osteonecrosis ofthe femoral head: comparison of radiography, CT, and MR imaging. AJRAm J Roentgenol 2003;180(2):363–8.

44] Fujioka M, Kubo T, Nakamura F, et al. Initial changes of non-traumaticosteonecrosis of femoral head in fat suppression images: bone marrowedema was not found before the appearance of band patterns. Magn ResonImaging 2006;19:985–91.

45] Kubo T, Yamamoto T, Inoue S, et al. Histological findings of bone marrowedema pattern on MRI in osteonecrosis of the femoral head. J Orthop Sci2000;5(5):520–3.

46] Rao VM, Fishman M, Mitchell DG, et al. Painful sickle cell cri-sis: bone marrow patterns observed with MR imaging. Radiology1986;161(1):211–5 [published erratum appears in Radiology 1987Jan;162(1 Pt 1):289].

47] Bonnerot V, Sebag G, de Montalembert M, et al. Gadolinium-DOTAenhanced MRI of painful osseous crises in children with sickle cell anemia.Pediatr Radiol 1994;24(2):92–5.

48] Cremin BJ, Davey H, Goldblatt J. Skeletal complications of type I Gaucherdisease: the magnetic resonance features. Clin Radiol 1990;41(4):244–7.

49] Vande Berg BC, Malghem J, Labaisse MA, Michaux JL, Maldague B.Apparent focal bone marrow ischemia in patients with marrow disorders:MR studies. J Comput Assist Tomogr 1993;17(5):792–7.

50] Ryu KN, Kim EJ, Yoo MC, Park YK, Sartoris DJ, Resnick D. Ischemic

necrosis of the entire femoral head and rapidly destructive hip disease:potential causative relationship. Skelet Radiol 1997;26(3):143–9.

51] Yamamoto T, Bullough PG. The role of subchondral insufficiency fracturein rapid destruction of the hip joint—a preliminary report. Arthritis Rheum2000;43(11):2423–7.