Pediatr Radiol (2013) 43:355–375
DOI 10.1007/s00247-012-2544-6
ORIGINAL ARTICLE
Chronic recurrent multifocal osteomyelitis (CRMO):
a longitudinal case series review
Céline Falip & Marianne Alison & Nathalie Boutry &
Chantal Job-Deslandre & Anne Cotten & Robin Azoulay &
Catherine Adamsbaum
Received: 3 April 2012 / Revised: 5 July 2012 / Accepted: 26 August 2012 / Published online: 22 December 2012
# Springer-Verlag Berlin Heidelberg 2012
Abstract
Background Chronic recurrent multifocal osteomyelitis
(CRMO) is an autoinflammatory disorder that is currently
diagnosed based on clinical, radiologic, pathological and
longitudinal findings.
Objective To provide detailed descriptions of CRMO lesion
patterns seen on radiographs and MRI and to suggest clin-
ical use of whole-body MRI and propose noninvasive diag-
nostic strategy.
Materials and methods Retrospective longitudinal study
(1989–2010) of 31 children (22 girls, 9 boys) diagnosed
with CRMO. Imaging data were evaluated by two pediatric
radiologists.
Results Mean age at diagnosis was 11 years (3–17). A total
of 108 lesions were investigated. The most common sites
were the long bone metaphyses (56 lesions in 24 children)
C. Falip
AP-HP, Pediatric Imaging Department,
St. Vincent de Paul Hospital,
Paris, France
M. Alison
Faculty of Medicine, Paris Diderot University,
Paris, France
M. Alison : R. Azoulay
AP-HP, Pediatric Imaging Department, Robert Debré Hospital,
Paris, France
N. Boutry : A. Cotten
Faculty of Medicine, Lille 2 University,
Lille, France
N. Boutry
Pediatric Imaging Department, Jeanne de Flandre Hospital,
Lille, France
especially femoral and tibial (20/24); pelvis (10/31); spine
(9/31); clavicle (6/31) and mandible (3/31). In long bones,
the radiologic appearance was normal (22/56), mixed lytic
and sclerotic (20/56), sclerotic (8/56) or lytic (6/56) often
juxtaphyseal (36/56), with hyperostosis or periosteal thick-
ening (10/56). Vertebral involvement was often multifocal
(6/9). Medullary edema was seen on MRI (42) with epiph-
yseal (23/42) or soft-tissue (22/42) inflammation and juxta-
physeal nodule-like appearance (7/42). Whole-body MRI
(15/31) was key in detecting subclinical lesions.
Conclusion CRMO is a polymorphous disorder in which
whole-body MRI is extremely useful for showing subclinical
edema. Vertebral collapse requires long-term monitoring.
Keywords Bone MRI . Inflammatory disease . Pediatrics .
Chronic recurrent osteomyelitis
C. Job-Deslandre
AP-HP, Rhumatology Department, Cochin Hospital,
Paris, France
A. Cotten
Musculoskeletal Radiology Department, Roger Salengro Hospital,
Lille, France
C. Adamsbaum
Faculty of Medicine, Paris Sud University,
Le Kremlin Bicêtre, France
C. Adamsbaum (*)
AP-HP, Pediatric Imaging Department, Bicêtre Hospital,
78 rue du Gal Leclerc,
94275, Le Kremlin Bicêtre Cedex, France
e-mail: c.adamsbaum@bct.aphp.fr
356
Introduction
Chronic recurrent multifocal osteomyelitis (CRMO) is a
type of skeletal inflammation occurring primarily in
childhood and adolescence, and more often in girls.
CRMO is often a diagnosis of exclusion in children
with multiple localized skeletal lesions. While the cause
and pathogenesis are still unknown, there is evidence
implicating both an autoinflammatory cause and genetic
susceptibility. Because none of the findings (clinical,
laboratory, radiographic or scintigraphic) is specific,
the diagnosis of CRMO remains a challenge. Though
numerous reports have focused on radiographic [1–16]
and MR patterns [7, 8, 12–15, 17, 18], few have de-
scribed the whole-body MRI findings [19, 20].
The objectives of this study are therefore:
– To provide detailed descriptions of CMRO lesion pat-
terns seen on radiograph and MRI
– To suggest a possible clinical use of whole body MRI in
this disease and propose an effective, non-invasive di-
agnostic strategy.
Materials and methods
This retrospective case study was conducted with three
pediatric imaging reference centers over an 11-year period
(1989–2010), and includes all children diagnosed with
CRMO (n031).
Children initially presented with local musculoskeletal
pain and/or swelling. Inclusion criteria were the following:
– child younger than 18 years,
– at least two localizations of osteitis or a recurrence of
osteitis in the same site
– and a surgical biopsy excluding an infectious or tumoral
process (n024) or a follow-up of 18 months or more (n07)
The diagnosis was based on clinical, laboratory and
radiologic findings and progression patterns in all 31
children, and on histological data obtained through bone
biopsy—either percutaneous or surgical—in 24 of them.
The complete record—including clinical, laboratory and
histological data—was reviewed and all imaging data
were analyzed by two experienced pediatric radiologists
(C.F. 7 years and C.A. 22 years).
Depending on the patients, the imaging studies included:
– Radiographs: two orthogonal views for all long bone
lesions and the spine, and at least one anteroposterior
view of the pelvis, clavicle and mandible.
– CT: at least one spiral acquisition with bone filter.
Pediatr Radiol (2013) 43:355–375
– Standard MRI: at least two different planes with two
different sequences, including T1-weighted spin-echo
(SE) and fat saturated T2 SE, or T1-weighted SE and
short-tau inversion recovery spin-echo (STIR). Contrast-
enhanced MRI was done for 19/31 children. At all three
centers, MRI was performed with a 1.5-T unit including an
Intera (Philips Healthcare, Best, The Netherlands), Signa
(GE Healthcare, Waukesha, WI) and MAGNETOM
Avanto (Siemens Healthcare, Erlangen, Germany)
– Whole-body MRI was performed with a combination of
phased-array coils. Body coverage was usually achieved
with four or five stations, which were combined to
obtain the whole-body image. Coronal T1-weighted
SE and STIR sequences were performed on all children.
At one center, sagittal T1-weighted SE and STIR
sequences were performed on the entire spine. None of
the children was sedated. The average examination time
was about 40 min.
Radiographs, CTs and MRIs were analyzed separately
using a reading grid. Images were evaluated for the presence
and number of bone lesions, after which each lesion was
categorized according to anatomical location. In tubular
bones, the site of each lesion was classified as either prox-
imal, middle or distal, and then either epiphyseal, metaphy-
seal, or diaphyseal [21]. The term “juxtaphyseal” was used
when the lesion was in contact with the growth plate. The
word “multifocal” indicates non-contiguous lesions. On
radiographs and CT scans, lesions were classified according
to their density (lytic, sclerotic or mixed), periosteal reac-
tion, and hyperostosis. On whole-body and standard MRI,
lesions were defined by abnormal signal intensity on both
STIR (high signal intensity) and T1-weighted SE (low sig-
nal intensity) images. Lesions were evaluated for location,
signal homogeneity and association with joint or/and soft-
tissue involvement.
The study methods were compliant with our institutional
ethics committee guidelines for retrospective observational
review study.
Results
The series included 22 girls and 9 boys, for a gender ratio of
2.4:1. The mean age at diagnosis was 11 years (range 3–
17 years). Three children had associated cutaneous lesions:
acropustulosis (n01), psoriasiform nail appearance (n01),
and furunculosis of the scalp (n01). None of the children
had an inflammatory gastrointestinal disorder. Regarding
laboratory findings, 2 children had a high leukocyte count,
9 children had elevated C-reactive protein (CRP), and 15
children had an elevated erythrocyte sedimentation rate
(ESR).
Pediatr Radiol (2013) 43:355–375 357

In 24 children, a biopsy was performed to rule out an Table 2 Percentage of children affected for each site (total number of
children n031)
infectious or tumoral process. One child underwent two
biopsies in the course of his disease. The site of the biopsy Sites n %
was in a long bone in 20 children, the mandible in 3 children
and a vertebra in 1 child. The histological and bacteriolog- Femur 13 42%
ical results from these bone biopsies showed a pattern sug- Tibia 12 39%
gestive of subacute or chronic osteomyelitis and no Pelvis 10 32%
microorganisms were isolated. In seven children, the clinical, Spine 9 29%
biological and radiographic features were initially suggestive Clavicle 6 19%
of CRMO and thereby, no biopsy was performed. The favor- Fibula 5 16%
able outcome under anti-inflammatory treatment retrospec- Tarsus (calcaneus: 4; talus: 3) 5 16%
tively confirmed the diagnosis in all of the children. The Radius 4 13%
mean follow-up was 5 years (range 18 months to 21 years). Ulna 4 13%
The mean number of pathological sites during the follow- Metatarsal 4 13%
up was 3.5 (range 1–14). Six children (19%) had only one Mandible 3 10%
disease focus, with recurrent pain at the same location (clav- Humerus 2 6.5%
icle, n02; tibia, n02; femur, n01; and mandible, n01). Patellae 1 3%
Twenty-five children (81%) had multifocal disease, i.e., at Carpus 1 3%
least two sites of CRMO. Rib 1 3%
In all, 108 bony locations were identified and imaged; Phalanx 1 3%
they were located, in descending order of frequency, in the
femur (18/108 in 13/31 children), the tibia (17/108 in 12/31
children), the spine (18/108 in 9/31 children), the pelvic
bones (12/108 in 10/31 children) and the clavicle (7/108 in overall, 64.5% (20/31) of children had femoral or tibial
6/31 children) (Tables 1 and 2) involvement sometime during the course of their disease.
A total of 56 long bone lesions were investigated:
Long bone involvement
– 46 symptomatic sites
Seventy-seven percent (24/31) of the children had involve- – 10 subclinical sites diagnosed by whole-body imaging
ment of at least one long bone during their illness. The bone (bone scan or MRI) and later studied by radiograph.
involved was the femur or tibia in 83% (20/24) of cases;
All 56 of those lesions were studied using radiographs;
11 were also studied by CT, and 42 by MRI.
Table 1 Distribution of disease sites Ninety-three percent (52/56) of the lesions were cen-
tered on the metaphysis. Involvement was juxtaphyseal
Sites (n0108) n %
in 64% (36/56) of cases. Extension into the diaphysis
Femur 18 16.5% was seen in 18% (10/56) of cases. Epiphyseal involve-
Spine 18 16.5% ment was seen frequently on MRI (55%, or 23/42), but
Tibia 17 16% rarely on radiograph (5%, or 3/56). Rarer still were
Pelvis 12 11% exclusively epiphyseal (n03) and exclusively diaphyseal
Clavicle 7 6.5% (n01) lesions.
Fibula 5 4.6% Radiographs were normal in 39% (22/56) of cases.
Tarsus (calcaneus: 4; talus: 3) 7 6.5% In the remaining 61% of cases, radiographs demon-
Radius 5 4.6% strated a focal lesion, either mixed, lytic or sclerotic.
Ulna 4 3.7% Thirty-six percent (20/56) of the lesions were mixed,
Metatarsal 4 3.7% i.e. both lytic and sclerotic. These tended to have two
Mandible 3 2.7%
distinct appearances: either several lytic elements within
Humerus 2 1.8%
an area of sclerotic bone (n014) (Fig. 1) or, less com-
Patellae 2 1.8%
monly (n06), a single lytic element surrounded by an
area of osteosclerosis, sometimes creating a “pseudo
Carpus 2 1.8%
nidus” appearance (Fig. 2). The other lesions were
Rib 1 0.9%
purely lytic (11%, 6/56) (Fig. 3) or purely sclerotic
Phalanx 1 0.9%
(14%, 8/56) (Fig. 4). The size of the lytic areas varied
358 Pediatr Radiol (2013) 43:355–375

Fig. 1 a Mixed lytic and

sclerotic lesion in the distal
humeral metaphysis in a
10-year-old boy. Note the
associated hyperostosis.
b Mixed lytic and sclerotic
juxtaphyseal lesion in the
proximal tibia of a
9-year-old girl

from a few millimeters to several centimeters. Lesions—
whether mixed or purely lytic—with a lytic component
were frequently juxtaphyseal (64%, 36/56). In eight
cases, this juxtaphyseal lysis made it look as if the
growth plate itself was widened (Fig. 5); in four cases,
this pseudo-widening was the only radiologic abnormal-
ity noted.
In addition to these focal lesions, diffuse bone abnormal-
ities were also noted in some of the children; there was
hyperostosis (Fig. 6) in 11% of cases (6/56), and periosteal
reaction (Fig. 7) in 7% of cases (4/56).
CT scan was used to explore long bone involvement
in 11 cases. In the majority of these cases (63%, 7/11),
the appearance on CT was consistent with the radiologic
appearance and no additional elements were found. In
two cases, CT scan revealed a lytic component, while
radiographs showed only sclerosis. In one case, CT
showed a mixed lesion, though the radiographs showed
only lysis; in another child, CT showed a mixed lytic
and sclerotic lesion involving both the tibia and the
distal fibula, while the radiograph showed only the
fibular lesion (Fig. 8).

Fig. 2 Nidus-like appearances

in the proximal left tibia (left)
and distal right femur (right) in
a 13-year-old girl. Note that the
lytic components are close to
the growth plates
Pediatr Radiol (2013) 43:355–375 359

MRI was used to investigate 42 long bone sites, and

revealed bone marrow edema in 100% of cases. In 90% (38/
42) of the cases, the lesions were centered on the metaphysis.
An associated edematous reaction in the epiphysis was
common (23/42, or 55%) (Fig. 9). On the other hand,
isolated diaphyseal or epiphyseal involvement was rare,
seen in only 1/42 and 3/42 children, respectively. In seven
children (17%), a juxtaphyseal nodule-like appearance
could be distinguished within the medullary edema, as a
very obvious hyperintense signal on the T2-weighted
images (Figs. 10 and 11). Inflammatory soft-tissue involve-
ment was frequent (52%, or 22/42), with a mass-like ap-
pearance in two cases (Figs. 12 and 13). No soft-tissue
collections could be seen. Associated joint effusions were
present in eight cases (19%) (Fig. 14). In one child this was
accompanied by synovial membrane contrast uptake, giving
the appearance of nonspecific synovitis.
The intravenous injection of contrast agent performed in
19 children demonstrated an enhancement, which was gen-
erally uniform; however, there was annular or nodular jux-
taphyseal uptake in seven children (Figs. 15 and 16).

Fig. 3 Juxtaphyseal osteolysis in the distal tibial metaphysis of an 8-
year-old girl
Spinal involvement
Nine children (29%, 9/31) had a spinal lesion sometime
during their illness. The spine was the presenting site of
involvement in four of them. In two children, the spinal

Fig. 4 Radiograph shows areas

of osteosclerosis involving
the distal end of the tibia, the
talus and the posterior calcaneus
of a 10-year-old boy (arrows)
360
Fig. 5 a Pseudo-widening of
the growth plate in the distal
fibula (arrow) in an 11-year-old
girl. b Pseudo-widening
of the growth plate in the left
femoral trochanter (arrow) in
an 8-year-old girl
lesions were completely asymptomatic, even as the disease
progressed. The most common clinical presentation was
stiffness of the spine, together with inflammatory pain.
Three of the children had kyphosis. The thoracic spine was
most frequently affected (78% of spinal sites, 14/18). None
of the lesions involved the cervical spine. While involve-
ment was often multifocal within the spine itself (in two-
thirds, or 6/9, of the children), in one case only, two contig-
uous vertebral bodies were involved.
In 55% (10/18) of the cases, the radiographs were nor-
mal. In the other cases (8/18) the vertebral end-plate had an
irregular, notched appearance that was often associated with
a loss of vertebral body height. In one of these, there was
frank vertebra plana.
Performed in four of the children, CT—as expected—
always demonstrated the mixed lytic and sclerotic appear-
ance of the lesion, as well as the notched appearance of the
vertebral end-plate. In one child, CT showed flattening of
the T3 vertebral body (vertebra plana) that was missed on
the radiographs due to the superposition of the humeral
heads (Fig. 17).
On MRI, osseous edema of the vertebral body was noted
in all of the cases where vertebral body height was pre-
served. When vertebral collapse was present, the signal was
variable. In two children there was a low signal intensity
line (T1 and STIR) parallel to the vertebral end-plate
(Fig. 18). Other abnormalities were observed here and there:
associated disk signal changes (two children), infiltration of
Pediatr Radiol (2013) 43:355–375
the perivertebral soft tissue (three children) less commonly
seen than in long bone involvement, involvement of the
neural arch (one child).
In the two children with vertebra plana, no recovery of
vertebral body height was observed (after an average of
18 months). No spinal cord compression or neurological
signs suggesting spinal cord or nerve root involvement were
observed.
Pelvic and pectoral girdle involvement
Pelvis
Eleven percent (12/108 lesions in 10/31 children) of sites
studied involved the pelvis. One-third of the children
thus had at least one iliac lesion in the course of their
illness. In more than half of the cases, these lesions
remained asymptomatic. They occurred either on the roof
of the acetabulum or in contact with the areas of syn-
chondrosis. Two of the children had associated involve-
ment of the sacroiliac joint (Fig. 19). The radiograph was
usually normal (9/12). Otherwise it showed a mixed lytic
and sclerotic lesion (n02) or a purely lytic lesion (n01).
One girl had iliac periosteal reaction associated with two
mixed lesions.
Out of the 12 lesions, 9 were studied with MRI and
showed bone marrow edema in all cases (Fig. 20).
Contrast uptake was generally uniform within the area
Pediatr Radiol (2013) 43:355–375
Fig. 6 Radiograph shows hyperostosis in the context of a mixed lytic
and sclerotic lesion in the ulnar metaphysis and diaphysis of a 13-year-
old girl
of edema. Soft-tissue infiltration could be seen in four
cases.
Clavicle
Six children had clavicular involvement during the course of
the disease; one child had simultaneous bilateral involve-
ment. In all cases, it was the inner third of the clavicle that
was involved. It was asymptomatic in only one child, where
it was discovered by whole-body MRI. No sternoclavicular
involvement or extension to the lateral end of the clavicle
was observed.
On radiograph, the most frequent presentation was scle-
rosis with hyperostosis (6/7). In two cases, lytic changes
361
Fig. 7 Radiograph shows Unilamellar periosteal reaction of the 4th meta-
tarsal in a 13-year-old girl (arrow). Note osteosclerosis and hyperostosis
were also seen. Periosteal reaction was common (3/7)
(Fig. 21). MRI showed bone marrow edema in all cases
(Fig. 22). All cases showed infiltration of the adjacent soft
tissue.
Mandibular involvement
Three of the children in our series exhibited mandibular
involvement. The appearance on imaging was either mixed
lytic and sclerotic (n02) or purely sclerotic (n01).
All three children had hyperostosis, which was particu-
larly striking in two of them, with facial deformity (Fig. 23).
In one of the children the lesion extended to the condyle,
with involvement of the temporomandibular joint. All three
cases showed inflammation of the adjacent soft tissue, and
two of them showed the appearance of a soft-tissue mass
with no collection (Fig. 24).
Other sites
– A single rib lesion was observed, on the posterior
costal arch of the right 7th rib. Radiograph and CT
showed osteolysis associated with a widening of the
costal arch. Periosteal reaction was visible, and
there was significant infiltration of the adjacent soft
tissue, marked by a filling in of the costovertebral
gutter (Fig. 25).
– Bilateral patellar involvement was observed in one child
in the form of purely sclerotic lesions on the radiograph.
MRI showed bone marrow edema with no extension
into the soft tissue (Fig. 26).
– Five children had involvement of the tarsus. Three children
had involvement of the calcaneus. The involvement was
362 Pediatr Radiol (2013) 43:355–375

Fig. 8 Value of CT in long bone lesions. Right ankle involvement in an 11-year-old girl. The radiograph shows a lytic juxtaphyseal lesion in the
distal fibula (arrow). CT scans reveal another lacular juxtaphyseal lesion in the distal tibia with subtle peripheral osteosclerosis (dotted arrow)

always posterior, in contact with the growth cartilage tissue. The Achilles tendon appearance remained normal.
(Fig. 27). All cases showed infiltration of the adjacent soft The talus involvement found in two children took the form

Fig. 9 Bilateral involvement of

the distal ends of the femur in a
10-year-old girl. a Radiograph
of the femurs shows mixed lytic
and sclerotic juxtaphyseal
lesions (arrows). b MRI, coro-
nal STIR sequence. Metaphy-
seal and epiphyseal osseous
edema
Pediatr Radiol (2013) 43:355–375
Fig. 10 Juxtaphyseal nodule of the femoral metaphysis in a 13-year-
old girl. In this sagittal T2-W fat-saturated MR image the signal
intensity of the nodule is higher than that of the adjacent osseous
edema
of isolated bone marrow edema, with no soft-tissue
abnormalities.
– One child had bilateral carpal involvement detected on
whole-body MRI; it was asymptomatic, and consisted
of isolated capitate bone marrow edema.
– Finally, one child had phalangeal involvement (1st pha-
lanx of the 2nd toe), studied by radiograph only. There
was a mixed lesion consisting of juxtaphyseal lysis,
sclerosis and hyperostosis.
Whole-body MRI
Fifteen children had a whole-body MRI scan. In 12 children
(80%), whole-body MRI disclosed a multifocal pattern of bone
lesions. It was decisive in the diagnosis of eight children,
showing subclinical inflammatory lesions (Figs. 28 and 29).
In two other children, whole-body MRI disclosed a symptom-
atic lesion that was not seen with radiographs (vertebra T11 and
tibia). The localizations seen with whole-body MRI were lo-
cated mainly within the metaphyses of long bones (six children)
and the pelvic bones (five children). Whole-body MRI dis-
closed spinal thoracic localizations that were subclinical in
363
Fig. 11 Another example of a juxtaphyseal fibular nodule in a 13-year-
old girl. Satittal T2-W fat-saturated MRI shows metaphyseal and epiph-
yseal osseous edema with a high signal intensity juxtaphyseal nodule.
Note the reactive inflammation in the adjacent soft tissue
two children. The lesions were bifocal in one child. Neither of
these two children was kyphotic. Five children had a bone scan
and a whole-body MRI within 2 weeks of each other. In four of
them, whole-body MRI revealed lesions that were missed on
bone scan because they were thought to be areas of physiolog-
ical uptake (Fig. 30). In all, 14 metaphyseal—or metaphyseal-
equivalent—lesions were missed on bone scan (proximal tibia,
n02; distal tibia, n02; carpus, n02; radius, n02; spine, n02;
pelvis, n02; fibula, n01 and femur, n01). In the fifth child, the
bone scan showed asymmetrical uptake in the sacroiliac joints,
for which whole-body MRI revealed a right sacral lesion with
no associated joint involvement.
Discussion
CRMO is seen mainly in children and adolescents. It is
characterized by recurrent non-bacterial osteomyelitis (NBO)
[12]. The metaphyses of the long bones, clavicles, spine and
pelvis are the sites most commonly affected [1, 4, 7, 13, 14].
The disease is marked by exacerbations and remissions and
the outcome at adulthood is generally good [6, 22–25].
CRMO was first described in 1972 by Giedion et al. [1],
who called it “chronic symmetrical osteomyelitis.” It was later
renamed CRMO by Gustavson et al. [26] and Probst et al.
364 Pediatr Radiol (2013) 43:355–375

Fig. 12 Femoral lesion in a 14-

year-old boy. Coronal (a) and
axial (b) STIR MR images
show a soft-tissue mass adja-
cent to the bone inflammation

[27], who found that the lesions were not always symmetrical.
Hundreds of cases have since been described in the literature
[3–16, 19].
The pathophysiology of the disease has not been
explained. The post-infectious origin suspected initially
has now been ruled out. No pathogen has been found, and
antibiotics have no effect on the course of the disease [5, 14,
16]. An autoimmune etiology has also been suggested, but
no significant antibodies have been found in these children.
Histological examination reveals nonspecific acute, sub-
acute or chronic osteomyelitis. Early lesions are character-
ized by a predominance of polymorphonuclear leukocytes
and osteoclastic bone resorption. Later, lymphocytes come
to predominate, along with new bone formation [28]. There

Fig. 13 Proximal tibial involvement in a 17-year-old girl. MRI, sag-

ittal T1-weighted fat-saturated MR image shows osseous edema cen-
tered on the growth plate of the anterior tibial tuberosity. Note the
inflammation of the adjacent soft tissue and infrapatellar bursitis Fig. 14 Distal tibial lesion in an 11-year-old girl. Sagittal T2-W fat-
(arrow) saturated MRI shows ankle joint effusion (arrow)
Pediatr Radiol (2013) 43:355–375 365

Fig. 15 Distal femoral lesion in a 13-year-old girl. Same child as in

Fig. 10. Coronal T1-W fat-saturated MRI after gadolinium injection
shows metaphyseal and epiphyseal osseous edema and annular contrast
uptake by the juxtaphyseal lesion. Note inflammation of the adjacent
soft tissue

are no histological markers that might be used to differenti-

ate CRMO from bacterial osteomyelitis.
CRMO is currently grouped with autoinflammatory dis-
orders like the SAPHO (synovitis, acne, pustulosis, hypeos-
tosis, osteitis) syndrome, of which it is thought to be the
juvenile form [29, 30]. Several observations and recent
studies suggest that genetic factors may play a role
[31–33]. As there is still no specific diagnostic test, the
principal differential diagnoses are acute bacterial osteomy-
elitis, bone tumors, blood diseases, fibrous dysplasia and Fig. 16 Distal fibular involvement in an 11-year-old girl. Coronal
T1-W fat-saturated MRI taken after gadolinium injection. Nodular
histiocytosis, and CRMO remains a diagnosis of exclusion
contrast uptake by the juxtaphyseal lesion (arrow) is more intense
with a relatively nonspecific clinical presentation. The diag- than that of the adjacent osseous edema. Note inflammation of adja-
nostic criteria usually used are [5, 6, 14]: cent soft tissue

– Multifocal bone lesions diagnosed clinically or radio-

graphically. In 19% of the cases in our series, how-
ever, there was a single focus, with recurrences at
that site [9, 12–14];
– A characteristic prolonged, fluctuating course with re-
current episodes of pain over several years;
– Sites that are atypical for infectious osteomyelitis, with
frequent clavicular involvement and multifocality;
– A radiographic picture suggesting subacute or chronic
osteomyelitis;
– No abscess formation, fistula or sequestra;
– Nonspecific histopathology and laboratory findings
consistent with subacute or chronic osteomyelitis;
– Lack of causative organism;
– Occasional association with pustulosis palmoplantaris
or acne;
– No response to antibiotic therapy, and improvement
with nonsteroidal anti-inflammatory drugs.
With no diagnostic markers and a relatively nonspe-
cific clinical presentation, CRMO diagnosis falls mainly
366
Fig. 17 Bifocal (T3/T9) involvement of the thoracic spine in a 10-
year-old girl (arrows). a Radiograph of the thoracic spine. T3 is not
visible due to superposition of the humerus. No significant T9 abnor-
mality is seen. b CT. Sagittal reconstruction. T3: Vertebra plana. T9:
notched appearance of the lower vertebral end plate with peripheral
Fig. 18 Multifocal spinal involvement in a 9-year-old girl. a Radio-
graph of the thoracic spine (lateral view). Loss of vertebral body
height, T4/T5/T6. Thoracic kyphosis. b Radiograph of the lumbar
spine (lateral view). L4: Loss of upper end plate cortical bone. Hetero-
geneous density of the vertebral body. c MRI, coronal T2-weighted
Pediatr Radiol (2013) 43:355–375
osteosclerosis; vertebral body height preserved. c MRI, sagittal T2-
weighted sequence with fat saturation. T3: vertebra plana, subtle bow-
ing of the posterior wall with no spinal cord signal abnormality. T9:
osseous edema of the vertebral body
sequence with fat saturation. L4: Osseous edema, small loss of verte-
bral body height. A low signal intensity rim parallel to the upper
vertebral end plate reflects bone impaction (arrow). Note concomitant
involvement of the left acetabulum and the right ischiopubic ramus
Pediatr Radiol (2013) 43:355–375
Fig. 19 Sacroiliitis in a
12-year-old girl. CT. Coronal
reconstruction shows widening
of the right sacroiliac joint
space (arrow). Bone erosion is
visible on the iliac side
to the radiologist, highlighting the importance of being
able to recognize the different imaging phenotypes. Our
study confirms a number of classic clinical and labora-
tory findings: mean age around 11 years and female
predominance [3, 4, 6, 9, 12–14, 16, 34, 35]; frequent, but
not inevitable, elevation in ESR (62% in our series) with
generally normal WBC and CRP [3, 6, 11, 13, 14, 16, 35,
36]; occasional associated skin involvement [8, 14, 25, 34,
35]; and nonspecific histopathology [1, 11, 12, 28, 36].
This study also confirms some classic radiologic features
[1–13, 16, 34]: in particular, the predilection for long bone
metaphyses (77%)—primarily femoral and tibial—and the
most common appearance at the time of diagnosis being a
mixed lytic and sclerotic juxtaphyseal lesion of variable size
[8–10, 13, 16, 27]. In particular, we stress the widening of
the growth plate, which may be isolated, regular, and very
subtle in the early stage of the disease. Left–right compar-
isons can be misleading due to the sometimes bilateral,
synchronous and symmetrical nature of the lesions, as in
four of our children. This sign, also described by Manson
[16], seems to us very specific to CRMO, and is easily
differentiated from the radiolucent juxtaphyseal bands that
are seen in leukemias or other general pathologies.
Hyperostosis and periosteal reaction are also suggestive
features, though less frequently observed.
Fig. 20 Right acetabular lesion
in a 9-year-old girl. a Radio-
graph. No abnormality is seen.
b Coronal T1-W MRI shows
osseous edema of the right ace-
tabulum (arrow)
367
Our study confirms the excellent sensitivity of MRI
in detecting CRMO lesions with bone marrow edema at
all but the spinal sites [12–15, 19]. While the area of
osseous edema is usually uniformly and moderately
enhanced, in some cases there can be more intense
nodular or annular juxtaphyseal contrast uptake—an ap-
pearance that, to our knowledge, has not been described
previously, though it appears in some illustrations [13].
This pattern of annular uptake is quite atypical in
CRMO and raises the question of an abscess, which
may look similar. However, we have never observed
the characteristic layered or target appearance reported
in Brodie’s abscess [37]. Our study also confirms the
presence of associated epiphyseal signal abnormalities in
more than half of the children studied [19]. This epiph-
yseal involvement, which is probably osseous edema, is
rarely visible on conventional radiographs [1, 4, 9, 16].
Generally speaking, bone inflammation is much more
extensive on MRI than radiographs would suggest [14,
15]. On the other hand, joint involvement seems fairly
rare (19%), though there are conflicting data on this in
the literature, where the number of cases is small and
the criteria for defining joint involvement are variable
(sometimes only clinical). Some authors have found
joint stiffness in as many as 50% of cases [6, 27, 38].
368 Pediatr Radiol (2013) 43:355–375

Fig. 21 Left clavicular lesion

in an 11-year-old boy. Radio-
graph shows osteosclerosis and
hyperostosis. A periosteal reac-
tion is visible on the lower edge
(arrow)

We found soft-tissue inflammation in 52% of children;
this was sometimes quite marked, creating an actual soft-
tissue mass. Such an appearance—probably underestimated
in the literature [7, 15]—should not rule out CRMO. Indeed,
Sundaram et al. [39] describes a soft-tissue mass with no
initial adjacent bone lesion. We never observed a soft-tissue
infiltration without an adjacent osteitic focus in our series.
Consistent with the literature, we found no cases of abscess
or soft-tissue fistula [7, 13–15]. This suggests that intrave-
nous contrast material is unnecessary in cases where CRMO
is certain or very likely.
Though spinal involvement is a classic finding in
CRMO, there is still debate about its frequency. Some
authors believe it is rare [6, 13, 18]. Others present it as
one of the most common sites [3, 4, 12, 17]. This lack of
agreement might be due to diagnostic underestimation. In

Fig. 22 Right clavicular lesion

in a 17-year-old girl. a Radio-
graph shows osteosclerosis and
hyperostosis of the inner half of
the clavicle. b Coronal T2-W
fat-saturated MRI shows het-
erogeneous clavicular edema
and signal abnormalities in the
adjacent soft tissue
Pediatr Radiol (2013) 43:355–375
Fig. 23 Mixed lytic and sclerotic lesion with hyperostosis of the
mandible in a 10-year-old boy. Panoramic dental radiograph
our study, 29% of children had spinal involvement some-
time during their illness. The thoracic spine is most often
affected in CRMO [9, 13, 17]. Spinal lesions are usually
multifocal and tend to involve non-contiguous vertebrae [9],
and the inflammation does not cross the disk [7, 15]. As
with long bone involvement, the vertebral lesions are usu-
ally mixed lytic and sclerotic; the vertebral end-plate is
irregular. Inflammation can lead to pathological verte-
bral body fracture, with vertebral collapse and MRI can
disclose a subchondral, fracture-like line parallel to the
vertebral end-plate together with altered bone marrow
signal intensity [18]. Vertebral collapse is unusual in
children and can be due to metastatic disease (lymphoma,
Fig. 24 Sclerosis and
hyperostosis in the ramus of the
right mandible in a 14-year-old
boy. Axial CT bone window (a)
and parenchymal window (b)
show mass in the contiguous
soft tissue
369
leukemia or neuroblastoma) or Langerhans histiocytosis.
Whole-body MRI combined with diffusion-weighted imaging
(DWI) can not only demonstrate other subclinical bone
lesions but also provide information about the cause of
the collapse, i.e. restricted diffusion in vertebral collapse
due to metastasis [40, 41]. The frequency of perivertebral
soft-tissue involvement varies in the literature [14, 22],
and was fairly rare in our series (16%) compared with
that near the long bones. One possible explanation might
be later diagnosis in these deep sites.
Clavicular lesions, as in the literature [1, 8, 9, 13–15, 42,
43], have a predilection for the inner third of the clavicle,
with no visible extension to the sternoclavicular joint—in
contrast to what is seen in SAPHO. The appearance on
imaging studies is marked by the frequent presence of
periosteal reaction (43%) and the significant hyperostosis
observed. MRI shows adjacent soft-tissue signal abnormal-
ities in all cases.
Pelvic lesions, which occurred in about one-third of the
children in this study, may be associated with sacroiliac joint
involvement (20%). As a reminder, synchondroses, which
are metaphyseal equivalents, are common sites of CRMO
involvement [15].
As already noted in the literature [13, 44, 45], mandibular
lesions, which were found in 10% of the children, can be
quite disfiguring.
Whole-body imaging is essential in CRMO, because
detection of subclinical foci of medullary edema is a
370 Pediatr Radiol (2013) 43:355–375

Fig. 25 Involvement of the

posterior arch of the right 7th
rib in a 9-year-old girl. a Ra-
diograph shows widening of the
posterior costal arch (arrow)
and thickening of the right par-
avertebral soft tissue. b Axial
CT shows lytic lesion of the
posterior costal arch, cortical
rupture and periosteal reaction.
c Axial T2-W fat-saturated MRI
shows infiltration of adjacent
soft tissue extending into the
costovertebral gutter

major diagnostic factor, and the increasing emphasis on
radiation dose reduction has made whole-body MRI the
advanced modality of choice. To date, the value of
whole-body MRI has been studied in pediatrics mainly
for oncological disorders and benign multifocal pathol-
ogies such as neurofibromatosis or dermatomyositis, and
whole-body MRI has received yet relatively little atten-
tion in the diagnosis of CRMO [40, 46–48]. Fritz [19]
reports excellent sensitivity of whole-body MRI in a
series of 13 CRMO children, where it showed “multi-
focality in all.” Not surprisingly, the sensitivity of
whole-body MRI is clearly superior to that of conven-
tional radiography. Relatively few authors have com-
pared the values of bone scintigraphy and whole-body
MRI (or even MRI) given the latter’s obvious perfor-
mance and the lack of radiation exposure in accordance
with the ALARA principle [20, 49]. The sensitivity of
whole-body MRI in detecting subradiological lesions
was always better than the sensitivity of bone scintigra-
phy, with the possible exception of extreme anterior and
posterior bone lesions, such as sternoclavicular and
costovertebral joints, which can be missed due to the

Fig. 26 Lateral radiograph

shows homogeneous sclerosis
of both patellae in a 10-year-old
boy (arrows)
Pediatr Radiol (2013) 43:355–375
Fig. 27 Lesion in the right
calcaneus of a 10-year-old boy.
a Radiograph shows osteolysis
of the posterosuperior angle of
the calcaneus (arrow). b Sagital
T1-W MRI shows osseous ede-
ma of the posterosuperior angle
of the calcaneus, in contact with
the growth plate. Note signal
abnormalities in the adjacent
soft tissue
technique of acquisition based on coronal planes [20].
In our series, whole-body MRI disclosed a multifocal
involvement in 80% of children. Five children had
whole-body MRI and a bone scan within 2 weeks of
each other. In four of them, whole-body MRI revealed
lesions that had been missed on scintigraphy because
they were located at metaphyseal or metaphyseal-equiv-
alent sites, which are areas of physiological uptake. In
the last case whole-body MRI demonstrated that the
uptake of the sacroiliac joint can correspond to sacral
edema even when the joint is spared. Finally, in all of
the children in whom we compared whole-body MRI
and scintigraphy, whole-body MRI provided additional
information and did not overlook any lesion seen with
scintigraphy. Moreover, MRI has excellent spatial reso-
lution, allowing an anatomical assessment of lesion ex-
tension in both bone and soft tissue at the same time,
and it can be used in children where pain recurs at a
previous site—a situation in which radiograph interpre-
tation can be difficult [47].
Whole-body MRI must include the entire body. T1-
weighted (either gradient-echo technique or turbo spin-
echo) and STIR imaging pulse sequences must be acquired
in the coronal plane to provide water-sensitive images that
can detect most lesions. DWI is a promising tool but yet not
evaluated in CRMO to the best of our knowledge. In this
retrospective study, DWI sequences were not performed.
Nevertheless, DWI sequences may have a potential role in
differentiating CRMO from a neoplastic disease in some
cases, such as a vertebral collapse. In general, diffusion of
water becomes restricted when there is a decrease in the
extracellular space, i.e. increase of membranes of tumors
and fibrosis. On the other hand, water diffusion is high when
the extracellular space increases as in vasogenic or inflam-
matory edema observed in infectious or inflammatory pro-
cesses [40, 41].
371
However, difficulties of interpretation related to suscepti-
bility artefacts and marrow conversion in young children must
be taken into account. In particular, the late physiological
persistence of hematopoietic marrow in the metaphyses that
are a main target of CRMO can be a pitfall [50]. Contrast
medium is not necessary at the time of the whole-body MRI. It
may be discussed at the time of standard localized MRI in
cases of doubtful findings such as pseudo abscess pattern.
In terms of diagnostic strategy, we agree with Gikas et
al. [8] and Fritz et al. [19] that, once CRMO is suspected,
bone biopsy should not be routine (Fig. 31). Indeed, when
the sites of involvement and radiographic appearance sug-
gest CRMO and the clinical and laboratory findings cor-
roborate this (good general health, relatively mild
inflammatory syndrome, moderately elevated ESR),
whole-body imaging is indicated. If whole-body MRI
confirms or reveals multifocality, radiographs of subclini-
cal sites are indicated. If the radiographic appearance is
also suggestive, a trial of anti-inflammatories with close
clinical supervision might be started. If symptoms resolve,
this would help confirm the diagnosis. The frequency of
radiograph checks and MRI follow-up needs to be deter-
mined prospectively. Finally, bone biopsy is indicated
only in cases where the clinical or radiologic findings
are inconclusive or multifocality has not been demonstrat-
ed. Its main purpose is to rule out other diagnoses, par-
ticularly infectious osteomyelitis, Langerhans histiocytosis
or malignant processes, depending on the presentation of
the child as previously discussed.
Several authors have studied the outcomes for CRMO
children in adulthood [6, 22–24, 51]. Though the pro-
longed, several-year course of the disease can disrupt
the child’s education, the long-term prognosis is good,
and the majority of children are asymptomatic as adults.
Among the complications that have been described in
the literature, several authors report persistent, disabling
372 Pediatr Radiol (2013) 43:355–375

Fig. 28 Multifocal
involvement in a 13-year-old
girl. The girl experienced left
2nd toe pain and left ankle pain,
2 weeks apart. a Radiograph
shows sclerosis and hyperosto-
sis in the proximal phalanx of
the left 2nd toe (arrow). b Ra-
diograph shows juxtaphyseal
osteolysis in the distal end of
the fibula (arrow). c, d Whole-
body MRI, sagittal STIR (c)
and coronal STIR (d) images
show asymptomatic inflamma-
tory foci in T4 (arrow in c), in
the right ala sacralis and the left
acetabulum (arrows in d)

clavicular hyperostosis that in some cases caused neuro-
vascular compression (thoracic outlet syndrome) [13,
24]. A few cases of leg length inequality have also
been described, secondary to premature epiphyseal fu-
sion. The most common and troublesome complications
are spinal. One case of spinal cord compression has
been described in the literature [52], and we found
kyphosis at the time of diagnosis in three children.
Several authors have also reported thoracic spine defor-
mities (kyphosis and scoliosis), underlining the need for
monitoring—probably long-term—at a frequency that
remains to be determined. The three children in our
Pediatr Radiol (2013) 43:355–375 373

Fig. 29 Multifocal involvement in a 10-year-old girl. Initial symptomatic lesions were located in the thoracic spine (illustrated in Fig. 17). Whole-
body MRI showed additional subclinical lesions (arrows) in the left acetabulum (a), distal right tibia (b) and in both distal femurs (c)

series were still kyphotic after 18 months of follow-up. [11, 13, 18]. Like Fritz et al. [19], we believe that it is
In addition, vertebral bodies do not seem to return to very important to detect spinal lesions as early as possible,
their initial height once the disease has run its course at the subclinical stage, in order to quickly start appropriate

Fig. 30 Chronic recurrent

multifocal osteomyelitis
(CRMO) in an 11-year-old boy.
Symptomatic lesions in the
mandible and right humerus. a
Technetium-99 m scintigraphy
shows increased humeral and
mandibular uptake. Note
asymptomatic inflammatory fo-
ci in both patellae and tarsi. b, c
Whole-body MRI (b) and cor-
onal STIR (c) images reveal
additional inflammatory foci in
the proximal and distal tibial
metaphyses (circles) not found
by scintigraphy
374
Fig. 31 Proposition for a diagnostic strategy
treatment like biphosphonates, which appear to be effective
in this indication [17]. It is also important to continue
clinical and radiologic monitoring (radiographs and MRI)
of the spine until growth is complete.
Conclusion
The two main imaging features to suggest the diagnosis of
CRMO are both the multifocal pattern of the lesions and
their sites—juxtaphyseal or physeal abnormal areas of den-
sity (femur and tibia), thoracolumbar spine, pelvic bones
and clavicle. A clavicular involvement is very suggestive of
CRMO but inconsistent. Imaging patterns can be various
and sometimes misleading, i.e. shaft thickening or epiphy-
seal involvement. Spinal involvement—observed in one-
third of children—should be recognized as soon as possible
to prevent long-term deformations. A pattern of vertebral
collapse must raise the possibility of CRMO as well as
neoplastic processes or Langerhans histiocytosis. On stan-
dard MRI, unusual CRMO patterns such as epiphyseal
involvement, enhancement of areas of edema and/or pres-
ence of soft-tissue mass should be recognized.
Currently, whole-body MRI is extremely useful in dem-
onstrating subradiologic lesions that are key signs for the
diagnosis of CRMO, thereby reducing the need for invasive
Pediatr Radiol (2013) 43:355–375
diagnostic procedures. Morever whole-body MRI helps
radiologists choose the best site for a biopsy if needed.
The role of whole-body MRI in therapeutic decision-making
and in clinical follow-up need to be established.
Acknowledgment The authors thank Pascale Zerbini for manuscript
preparation.
Conflict of interest None
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