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

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DOI: 10.1016/j.ejrad.2008.01.061 · Source: PubMed
Abstract
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 kept in mind that this syndrome should be regarded, not as a specific diagnosis, but rather as a sign of an ongoing abnormal process that involves the 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-specific finding on T1-weighted images and by focusing on ancillary findings on T2-weighted SE or fat-saturated proton-density weighted MR images.
European Journal of Radiology 67 (2008) 68–77
Bone 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, Universit´e 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
Abstract
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
kept in mind that this syndrome should be regarded, not as a specific diagnosis, but rather as a sign of an ongoing abnormal process that involves
the 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-specific
finding 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.
Keywords: Bone marrow; Edema; Femoral head; Osteoporosis; Osteonecrosis
The phrase “bone marrow edema”, is routinely used in clin-
ical practice to indicate the presence of a pattern of marrow
alteration that is common to numerous bone and joint disorders
[1,2]. The current article focuses on the definition and differ-
ential diagnosis of the bone marrow edema syndrome of the
femoral head.
1. The bone marrow edema syndrome of the femoral
head
The “bone marrow edema syndrome” of the femoral head is a
generic term used to refer to a lesion pattern seen at MR imaging
and characterized by altered marrow signal intensity within the
femoral head suggestive of medullary infiltration by interstitial
edema [3–5] (Fig. 1).
Four morphologic criteria on T1-weighted SE images indi-
cate the presence of the bone marrow edema syndrome of the
femoral head (Table 1). First, the lesion must involve the femoral
head. It generally involves the upper pole and reaches the sub-
chondral bone [5,6]. It may extend into the femoral neck and,
rarely, subtle marrow changes also involve the acetabulum. Sec-
ond, the lesion lacks definite margins and the transition zone
between 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).
the lesion signal is homogeneous, without obvious focal round
or lobulated changes and without residual intralesional fatty
areas. Finally, the lesion signal intensity is moderately reduced
on T1-weighted SE images. All these features must be seen
on T1-weighted images. The lesion’s signal intensity is inter-
mediate to high on T2-weighted SE images and high on STIR
and fat-saturated intermediate- or T2-weighted images. After
intravenous contrast injection, homogeneous and moderate to
marked signal intensity enhancement is seen on T1-weighted
SE images [5,8]. At close inspection of these sequences, subtle
focal changes can occasionally be detected in the subchondral
area. These additional changes may represent clues to a more
specific diagnosis (Table 2). A moderate joint effusion is usually
present. The adjacent soft tissues are generally normal.
Epidemiological data on the bone marrow edema syndrome
are sparse. In a consecutive series of 60 patients with a transient
bone marrow edema syndrome of the femoral head, there were
Table 1
Morphological criteria of the bone marrow edema of the femoral head on T1-
weighted SE MR images
Topography At least femoral head (subchondral area), also in
femoral neck
Margins Ill-defined margins, no peripheral rim
Overall appearance Homogeneous, no high or low signal foci in the
lesion
Signal intensity Moderately reduced
0720-048X/$ – see front matter © 2008 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.ejrad.2008.01.061
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 signal
intensity that predominates in the subchondral region and also involves the femoral neck. The lesion is ill-delimited. Another lesion with sharp margins and more
pronounced and homogeneous decrease in signal intensity involves the femoral neck. The latter lesion is unlikely to represent marrow edema. (b) The corresponding
T2-weighted SE image shows intermediate signal intensity in the femoral head and moderate joint swelling. (c) The sagittal T1-weighted SE image of the femoral
head 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 located
at 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 spontaneously
disappeared at MR follow-up, whereas the femoral neck lesion remained unchanged.
Table 2
MR 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) Irreversible
Frank femoral head deformity Osteonecrosis (rarely osteoarthritis) Irreversible
Subchondral cleft fracture
a
Osteonecrosis (rarely osteoarthritis) Irreversible
Crescent-shaped low signal intensity subchondral area Osteonecrosis, osteoarthritis, insufficiency fracture Variable
b
Subchondral impaction fracture
c
Insufficiency fracture or transient osteoporosis Reversible
No 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) Coronal
T1-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 edema
syndrome. (c) Sagittal T1-weighted SE image shows that the abnormal signal predominates in the subarticular area. The acetabular bone is normal. (d) The abnormal
marrow demonstrates high signal intensity on the corresponding T2-weighted SE image. (e) The sagittal T1-weighted SE image obtained several months later
demonstrates a return to a normal signal pattern.
B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77 71
Table 3
MR 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 plate
Orientation Parallel to bone plate variable
Morphology Thin, short Large, serpiginous
T2-weighted images Low signal Double-line sign
Enhanced T1-weighted Low signal, better seen than on SE T1 Less well seen than on SE T1
Most prominent on Fat-saturated proton density T1-weighted SE
37 male and 23 female patients with a mean age of 49 and 48
years, respectively [9]. In this series, about half of the lesions
were observed in association with various medical conditions
including pregnancy, glucocorticoid therapy, alcohol abuse, and
metabolic bone diseases.
At histology, the most characteristic feature of bone mar-
row edema syndrome of the femoral head is focal area of thin
and disconnected bone trabeculae covered by osteoid seams and
active osteoblasts with formation of irregular woven bone (cal-
lus) [10]. The surrounding bone marrow tissue shows edematous
changes and mild fibrosis, frequently associated with fat cell
destruction, vascular congestion and/or interstitial hemorrhage.
No osteonecrotic region is observed in either the bone trabeculae
or the bone marrow tissue. In addition to increased osteoid vol-
ume, a decreased maximal hydroxyl apatite content and a shift
to undermineralized bone can be found by mineral densitometry
[11].
The pathophysiology of the bone marrow edema syndrome
remains unknown. Links with ischemia, fractures and reflex
sympathetic dystrophy syndrome have been suggested. From
a clinical point of view, it is important to keep in mind that
the bone marrow edema syndrome is non-specific and probably
results from different causes [12]. Subsequently, the bone mar-
row edema syndrome of the femoral head shows a variable time
course, depending on theunderlying causes that include transient
osteoporosis of the hip [3,13], idiopathic bone marrow edema
of the hip [4,6], traumatic or stress fracture of the femoral head
[14,15], hip osteoarthritis [16–18] and femoral head osteonecro-
sis [19,20]. The distinction between these conditions is crucial
because of their different outcomes [6]. Transient osteoporo-
Fig. 3. Migratory bone marrow edema syndrome. (a) Coronal T1-weighted SE image of the pelvis of a 67-year-old man with left hip pain shows the bone marrow
edema syndrome of the left femoral head. (b) Two months later, a follow-up coronal T1-weighted SE image shows disappearance of the lesion. (c) Eleven months
after the initial study, right hip pain appeared and a coronal T1-weighted SE image of the pelvis showed the bone marrow edema syndrome in the right femoral head.
72 B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77
sis and idiopathic bone marrow edema syndrome are generally
spontaneously self-limited. Insufficiency stress fracture may
either completely resolve or progress toward epiphyseal collapse
[21]. Finally, hip osteoarthritis and femoral head osteonecro-
sis are not spontaneously reversible and can lead to joint
failure.
2. Transient osteoporosis of the hip
Transient osteoporosis of the hip is an uncommon clini-
cal entity characterized by the spontaneous appearance and
resolution over time of hip pain and the associated delayed
appearance of marked osteoporosis of the femoral head [22,23]
(Fig. 2). MR imaging does not enable recognition of this pecu-
liar entity but its widespread use has facilitated the detection of
the bone marrow edema syndrome that is observed in transient
osteoporosis.
This condition generally involves adult male patients with a
typical time course of clinical and radiographic changes. Unilat-
eral hip pain begins spontaneously, may be rapid or gradual in
onset and is aggravated by weight-bearing. After a plateau phase,
pain progressively decreases until complete regression by 6–12
months after the onset, without residual sequelae. Initial radio-
graphs are normal, but marked osteoporosis of the femoral head
with preserved joint space is seen on radiographs obtained sev-
eral weeks after the onset of symptoms. The bone resorption can
be so intense that the subchondral bone plate becomes indistin-
guishable on conventional radiographs. Follow-up radiographs
demonstrate a return to a normal appearance. Radionuclide
studies with bone-seeking agents reveal abnormal accumula-
Fig. 4. Femoral head osteonecrosis. (a) A coronal T1-weighted SE image shows the bone marrow edema syndrome in the femoral head. Note that the signal of the
lesion is very low. (b) A sagittal fat-saturated intermediate-weighted images shows the presence of a subchondral crescent-shaped low signal intensity area (arrow)
in the antero-superior aspect of the femoral head, indicative of necrosis. Note that the cartilage appears normal. (c) Follow-up radiograph obtained 3 months later
shows femoral head osteonecrosis with marked epiphyseal collapse.
B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77 73
tion of isotope in the femoral head. At MR imaging, the bone
marrow edema syndrome is observed [3,5,13]. The severity
of osteopenia does not correlate with the extent of marrow
edema [24]. Discrete additional changes can be seen in the
subchondral area, including low signal intensity lines and sub-
tle depression of the subchondral bone plate in some or the
majority of cases of transient osteoporosis of the femoral head
[25].
In general, the diagnosis of transient osteoporosis of the
femoral head remains presumptive, until demonstration of com-
plete resolution of clinical and radiological changes. Transient
osteoporosis does not recur in the same joint but may involve
another lower limb epiphysis, a situation called migratory tran-
sient osteoporosis (Fig. 3).
3. Insufficiency or stress fractures of the femoral head
Fractures of the trabecular bone of the femoral head are
an ubiquitous finding observed in resected specimens for
osteoarthritis, arthritis, avascular necrosis, transient osteoporo-
sis and rapidly destructive osteoarthritis [21]. The concept of
isolated trabecular fatigue (normal stress weakened bone) of
the femoral head has progressively emerged during the last 15
years, thanks to the use of MR imaging [14,15,26–30]. Insuffi-
Fig. 5. Typical femoral head osteonecrosis and marrow edema in a 23-year-old woman with steroid therapy. (a) Coronal T1-weighted SE image of both hips shows
abnormal signal in the left femoral head and neck. (b) On a coronal T1-weighted image, marrow edema predominates in the femoral neck. A rim of low signal
(arrow) separates the proximal lesion from the infiltrated marrow. (c) On the corresponding T2-weighted SE image, the lesion is barely visible. The femoral neck
marrow shows intermediate signal intensity. This lesion pattern is indicative of femoral head osteonecrosis. (d) Three months later, a coronal T1-weighted image
shows collapse of the left femoral head with low signal in the lesion and a normal femoral neck marrow.
74 B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77
ciency fractures of the femoral head is one of the cause of the
bone marrow edema syndrome of the femoral head (Fig. 1). In
addition to bone marrow edema, two morphological changes are
diagnostic clues for insufficiency fractures, although they can
also be observed in transient osteoporosis [24]. In insufficiency
fractures, marked and focal osteopenia is generally lacking on
radiographs.
First, impaction fractures of the trabecular bone appear as
thin low signal intensity bands or lines or more globular speckled
areas of low signal intensity on the T2- or enhanced T1-weighted
SE images. They should not be confused with the reactive inter-
face or rim that surrounds marrow infarcts (Table 3). The plane
of impaction fractures runs parallel to the subchondral bone
plate at a small distance from the articular surface and does
not delineate a large marrow area [31]. It is surrounded by mar-
row edema on both sides (with no residual fat in the subchondral
area) and it does not show the double-line sign on T2-weighted
spin-echo images. These lines are generally more prominent on
T2-weighted than on T1-weighted sequences.
Second, subtle focal deformity of the subchondral bone
plate is occasionally visible in the antero-superior or lateral
aspects of the femoral head, just below the acetabular roof
margin. This probably represents discrete impaction of the
bone plate separating the articular cartilage from the under-
lying bony trabeculae. These depressions of the subchondral
bone plate remain limited and are not as abrupt or as marked
as the overt fractures that occur in epiphyseal osteonecro-
sis. They can be better seen on intermediate-weighted SE
images or contrast-enhanced T1-weighted SE images probably
due to a high signal contrast between marrow and carti-
lage.
4. Femoral head osteonecrosis
Extensive marrow edema can be observed in femoral head
osteonecrosis in at least three different situations. First, femoral
head osteonecrosis can develop as an isolated predominant
finding, mainly in elderly patients, in a manner reminiscent to
Fig. 6. Osteoarthritis and bone marrow edema syndrome in a 74-year-old woman. (a) Radiograph of the pelvis shows joint space narrowing of the left hip without
osteophytes. (b) Coronal T1-weighted SE image shows abnormal femoral head marrow, joint swelling but normal acetabular marrow. (c) Sagittal fat-saturated
intermediate-weighted image shows narrowing of the anterior joint space and abrasion of the cartilage. Marrow edema of the femoral head marrow is most likely
related to the development of cartilage abrasion. Total hip replacement was performed a few months later.
B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77 75
that of spontaneous osteonecrosis of the knee (Fig. 4). This
lesion pattern represents about 10% of symptomatic femoral
head osteonecrosis [5,7,19,32]. It is observed in patients without
known risk factors for avascular necrosis and is usually not
associated with marrow infarcts in other bones. On T1-weighted
SE images, there is no residual fat within the necrotic lesion and
there is no interface at its periphery. In this case of the bone mar-
row edema syndrome, careful analysis of the subchondral area
on T2- or fat-saturated intermediate-weighted images usually
shows additional features suggestive of epiphyseal osteonecro-
sis. First, a crescent-shaped low signal intensity area is seen in
the subchondral area, delineated at its lower aspect by edema.
This low signal intensity area is reminiscent to that of necrotic
tissue observed in classic forms of epiphyseal osteonecrosis
[33–35] and in spontaneous osteonecrosis of the knee. Second,
femoral head deformity can be observed and indicates epiphy-
seal collapse compatible with femoral head osteonecrosis. These
additional changes are barely visible on the T1-weighted SE
images.
Unfortunately, these two changes are not specific and can
also be observed in insufficiency stress fractures and transient
osteoporosis. To some extent, determination of their importance
contributes to differentiate irreversible (osteonecrosis, some
insufficiency fractures) from reversible lesions (transient osteo-
porosis, some insufficiency fractures). A low signal intensity
subchondral area with a thickness equal or superior to 4 mm (in
other words, thicker than the articular space) on T2-weighted
images suggests an irreversible lesion with a specificity of about
92% [9]. Marked femoral head contour deformity also indicates
osteonecrosis but this feature can be difficult to assess on cross
sectional images.
Second, in systemic osteonecrosis (the condition observed in
patients with multiple marrow infarcts associated with inflam-
matory diseases, alcohol abuse or steroid treatment) and in
post-traumatic osteonecrosis, extensive head and neck edema
can occur [36–40] (Fig. 5). In this condition, a focal ischemic
lesion involves the upper pole of the femoral head, and marrow
edema occurs more distally, in the femoral head and neck and
spares the proximal lesion. Therefore, this lesion pattern does
not correspond to a true bone marrow edema syndrome. The T1-
weighted SE image better displays the ischemic femoral head
lesion because this lesion contains residual marrow fat and is sur-
rounded by a low signal intensity rim. Many authors agree on
the hypothesis that marrow edema distal to a subchondral infarct
is an indirect sign of epiphyseal fracture [40–43], although oth-
ers believe that edema represent progressive ischemia. Other
studies also indicated that this typical pattern of femoral head
osteonecrosis is not preceded by marrow edema [44,45].
Finally, femoral head osteonecrosis can also show bone mar-
row edema in patients with haematological conditions or reactive
haematopoietic marrow hyperplasia [46–49]. In this situation,
the entire marrow is abnormal and the lesion develops in a
red-marrow equivalent area and not in yellow marrow.
5. Osteoarthritis
Osteoarthritis of the hip can generally be recognized by
the presence of subchondral cysts, subchondral bone sclerosis
Table 4
Flow chart for systematic analysis of the bone marrow edema syndrome of the femoral head femoral head indicating sequences, possible focal lesions, prognosis
and most likely diagnoses
76 B.C. Vande Berg et al. / European Journal of Radiology 67 (2008) 68–77
and, at close inspection, focal or extensive cartilage changes.
These changes generally involve both the acetabulum and the
femoral head. However, in some unusual cases, hip osteoarthri-
tis shows the bone marrow edema syndrome (Fig. 6). This lesion
pattern has been recognized in rapidly progressive osteoarthri-
tis, a condition which can rapidly lead to joint destruction
[16–18]. In rapidly progressive osteoarthritis, a combination
of bone and marrow changes can be seen, including defor-
mity of the subchondral bone plate, impaction fractures of
the trabecular bone and extensive marrow infiltration. Gener-
ally, marginal osteophytes are absent. The presence of cartilage
abrasion is the diagnostic clue, but it may be difficult to rec-
ognize. This lesion pattern is very similar to that of epiphyseal
osteonecrosis. In osteonecrosis, cartilage abrasion parallels the
degree of epiphyseal deformity, although massive femoral head
infarction can rapidly cause proximal femur destruction [50].
Hypothetically, cartilage lesion could develop early in the dis-
ease course in rapidly evolving osteoarthritis and could be
followed by the development of bone fracture and marrow edema
[21,51].
6. Recommended analysis pattern of MR images of
femoral head bone marrow edema
A careful and systematic analysis of the MR images is rec-
ommended when facing the bone marrow edema syndrome of
the femoral head, given the variable outcomes observed in the
numerous conditions showing this syndrome [12] (Table 4).
First, analysis of the T1-weighted SE images is mandatory
to differentiate a true “bone marrow edema syndrome” from
other lesions in which marrow edema can also be a predominant
feature like tumors, infection, cysts and systemic osteonecrosis.
Second, after confirmation of the bone marrow edema syn-
drome on T1-weighted SE images, high-resolution T2-weighted
SE sequences are useful to assess (a) the articular cartilage,
(b) the subchondral bone plate and (c) the subchondral mar-
row. Several rules are useful: (a) if the articular cartilage
is abnormal, the lesion is clinically irreversible (osteoarthri-
tis or osteonecrosis); (b) if the subchondral bone plate is
interrupted and the epiphysis lacks sphericity, the lesion is
irreversible; (c) if a fluid-like signal intensity plane is visible
underneath the epiphyseal contour (cleft fracture), the lesion is
irreversible.
Finally, after exclusion of a cartilage lesion and obvious frac-
ture of the subchondral bone plate, detection and quantitative
assessment of possible focal subchondral changes (low signal
intensity subchondral area on T2- or enhanced T1-weighted SE
images), may yield information relevant to the spontaneous out-
come of these lesions. The lack of any additional focal changes
in the subchondral edematous marrow area indicates a favorable
prognosis, i.e. spontaneous resolution of the lesions and symp-
toms. The presence of a crescent-shaped low signal intensity
area in the subchondral region with a thickness equal or supe-
rior to 4 mm on T2-weighted images suggests an irreversible
lesion. In some situations, the prognosis remains uncertain and
follow-up MR studies obtained 3 months later represent a valid
alternative to further evaluate the femoral head lesion.
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    • "This low-intensity band in SIF was histologically proven to correspond with the fracture line and associated repair tissue [5, 9]. Some cases of SIF resolve after conservative treatment [5,11121314; other cases progress until collapse, thereby requiring surgical treatment45678910 15]. The prognosis of SIF patients remains unclear. "
    [Show abstract] [Hide abstract] ABSTRACT: The aim of this study was to identify the risk factors associated with the prognosis of a subchondral insufficiency fracture of the femoral head (SIF). Between June 2002 and July 2009, 25 patients diagnosed with SIF were included in this study. Sequential radiographs were evaluated for the progression of collapse. Clinical profiles, including age, body mass index, follow-up period and Singh's index, were documented. The morphological characteristics of the low-intensity band on T(1) weighted MRI were also examined with regards to four factors: band length, band thickness, the length of the weight-bearing portion and the band length ratio (defined as the proportion of the band length to the weight-bearing portion of the femoral head in the slice through the femoral head centre). Radiographically, a progression of collapse was observed in 15 of 25 (60.0%) patients. The band length in patients with progression of collapse [22.5 mm; 95% confidence interval (CI) 17.7, 27.3] was significantly larger than in patients without a progression of collapse (13.4 mm; 95% CI 7.6, 19.3; p<0.05). The band length ratio in patients with progression of collapse (59.8%; 95% CI 50.8, 68.9) was also significantly higher than in patients without a progression of collapse (40.9%; 95% CI 29.8, 52.0; p<0.05). No significant differences were present in the other values. These results indicate that the band length and the band length ratio might be predictive for the progression of collapse in SIF.
    Full-text · Article · Mar 2012
    • "La distinction est importante car les fractures ont un pronostic plus souvent favorable que les nécroses. C'est parfois la seule évolution qui permet le diagnostic définitif des images initialement ambiguës [37]. "
    [Show abstract] [Hide abstract] ABSTRACT: In 1892, J. Wolff, an orthopedic surgeon, stated that the internal architecture and shape of a bone were related to the direction of stresses placed upon it. Conventional radiographs and MRI can demonstrate the adaptability of bones to stresses. Imaging also demonstrates that this adaptability has limitations, and that excessive stress may lead to fracture. Copyright © 2011 Elsevier Masson SAS and Éditions françaises de radiologie. All rights reserved.
    Article · Mar 2011
  • Full-text · Article · · Journal de Radiologie
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