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European Journal of Radiology 136 (2021) 109533

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European Journal of Radiology


journal homepage: www.elsevier.com/locate/ejrad

Research article

Whole-body magnetic resonance imaging in inflammatory diseases: Where


are we now? Results of an International Survey by the European Society of
Musculoskeletal Radiology
Chiara Giraudo a, *, Frederic E. Lecouvet b, Anne Cotten c, Iris Eshed d, Lennart Jans e,
Anne Grethe Jurik f, Mario Maas g, Michael Weber h, Iwona Sudoł-Szopińska i
a
Radiology Institute, Department of Medicine – DIMED, University of Padova, Italy
b
Department of Radiology and Medical Imaging, Institut de Recherche Expérimentale et Clinique (IREC), Université Catholique de Louvain (UCL), Cliniques
Universitaires Saint Luc, Brussels, Belgium
c
Department of Musculoskeletal Radiology, Lille University Hospital, Lille, France
d
Department of Radiology, Sheba Medical Center, affiliated with the Tel Aviv University, Tel Aviv, Israel
e
Department of Radiology and Medical Imaging, Ghent University Hospital, Ghent, Belgium
f
Department of Radiology, Aarhus University Hospital, Aarhus N, Denmark
g
Department of Radiology, Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands
h
Department of Biomedical Imaging and Image-Guided Therapy, Medical University of Vienna, Vienna, Austria
i
Department of Radiology, National Institute of Geriatrics, Rheumatology and Rehabilitation, Warsaw, Poland

A R T I C L E I N F O A B S T R A C T

Keywords: Purpose: To investigate the current role of WB-MRI for rheumatic inflammatory diseases in clinical practice using
Whole Body Imaging a survey addressed to musculoskeletal radiologists.
Magnetic resonance imaging Methods: A survey composed of 61 questions, subdivided in three sections, demographics (five questions),
Rheumatic diseases
application of WB-MRI for inflammatory musculoskeletal diseases in adults and children (28 questions: 7 open
and 21 multiple choice for each subgroup) was distributed via the European Society of Musculoskeletal Radi­
ology (ESSR) from July 2 to December 31, 2018 to radiologists working in academic, private, and public
workplaces. Comparisons among the different workplaces were performed using the Chi-squared and the
Kruskal-Wallis test for nominal and ordinal data, respectively (p < 0.05).
Results: Seventy-two participants out of the 1779 (4%) members of the ESSR with 10.4 ± 7.9 years of experience
in musculoskeletal imaging, replied to at least one question. 30.6% and 12.3% of the respondents performed at
least 50 WB-MRI examinations per year in adults and children, respectively. The most frequent indications were
myositis in adults and chronic recurrent multifocal osteomyelitis (CRMO) in children, the latter mostly in aca­
demic centers (p = 0.013). The ESSR Arthrits Subcommitte’s protocol was applied by half of the participants and
especially radiologists working in private practice used it for adults (p = 0.025). Contrast medium was rarely
used for adults particularly by academics (p = 0.04). Diffusion Weighted Imaging was applied for children mostly
in private practice (p = 0.01) although, overall, it plays a marginal role. Scoring systems were rarely used.
Ongoing research is limited.
Conclusion: WB-MRI is not routinely applied for musculoskeletal inflammatory diseases. The most frequent in­
dications are myositis and CRMO.

1. Introduction imaging (MRI) allows a reliable anatomical characterization, an accu­


rate detection of active inflammation, and a precise assessment of the
Numerous inflammatory diseases may affect the different compo­ response to treatment [2–4]. Indeed, over the past decades, MRI has
nents of the musculoskeletal system [1]. Because of its high contrast become the modality of choice for several rheumatic diseases [5]. It has
resolution for bone marrow and soft tissues, magnetic resonance revolutionized the management of spondyloarthritis allowing early

* Corresponding author at: Institute of Radiology, Department of Medicine – DIMED, Padova University, Via Giustiniani 2, 35100, Padova, Italy.
E-mail address: chiara.giraudo@unipd.it (C. Giraudo).

https://doi.org/10.1016/j.ejrad.2021.109533
Received 4 February 2020; Received in revised form 7 December 2020; Accepted 5 January 2021
Available online 9 January 2021
0720-048X/© 2021 Elsevier B.V. All rights reserved.
C. Giraudo et al. European Journal of Radiology 136 (2021) 109533

diagnosis [6]. MRI is also the first line technique for idiopathic inflam­ (five questions), application of WB-MRI for inflammatory musculoskel­
matory myositis (IIM) and other less frequent conditions involving etal diseases in adults and children (28 questions: 7 open and 21 mul­
fasciae and muscles, like systemic sclerosis [7,8]. Furthermore, MRI tiple choice for each category).
plays a major role in pediatric inflammatory diseases such as chronic The questionnaire was introduced by a short description of the
recurrent multifocal osteomyelitis (CRMO), juvenile dermatomyositis or project, highlighting that the survey would have taken around 10 min
polymyositis, and juvenile idiopathic arthritis (JIA) [9,10]. and that the project managers (CG and IS) were available for further
Although most of the above-mentioned rheumatic diseases may information.
simultaneously affect various compartments of the musculoskeletal The survey was administered using the free platform Google Form
system, the recommended protocols usually cover limited areas of the (Google,Mountain View,CA) from July 2, 2018 and distributed by the
body. Recently, because of hardware and software developments, ESSR via newsletter to all 1779 Members. Data have been treated
whole-body MRI (WB-MRI) scans can be performed in a relative short anonymously; participants could provide their name which was not
time [11], representing a revolutionary diagnostic approach not only in linked to the collected data and has been shown in the
the oncological field [12–14]. The increasing interest for WB-MRI is well Acknowledgments.
demonstrated by the broad literature about its application for inflam­ A second and a third invitations after respectively one and two
matory arthropathies and muscle diseases [15–22]. Nevertheless, over­ months were sent out to further promote the participation.
all, little is known regarding WB-MRI current use and acceptance in On December 31, 2018 the survey was officially closed.
clinical practice. Moreover, while several studies recently addressed the
role of contrast medium and sequences like Diffusion Weighted Imaging
2.2. Statistical analyses
(DWI) and DIXON in WB-MRI [18,19], most of the proposed protocols,
including the one recommended by the Arthritis Subcommittee of the
After closure of the survey the collected answers were thoroughly
European Society of Musculoskeletal Radiology (ESSR), suggest the
analyzed. Answers to open questions were grouped according to the
application of T1w and Short Tau Inversion Recovery (STIR) sequences
thematic area.
only [21].
Descriptive statistics were applied for categorical data and results
The current paper reports the results of a survey supported by the
were mainly expressed as percentages, referring to the overall number of
ESSR, addressed to musculoskeletal radiologists, which aimed to obtain
respondents to each question.
a comprehensive overview about the current role of WB-MRI for in­
Aiming to provide a deeper insight into the application of WB-MRI in
flammatory rheumatic diseases in clinical practice as well as the fre­
different work environments, the answers were subdivided and
quency of its use, the most frequently targeted diseases, the areas of
compared according to the workplace (i.e., academic, private, and
ongoing research, and the applied protocols.
public). Comparisons among the different groups were performed using
the Chi-squared and the Kruskal-Wallis test for nominal and ordinal
2. Materials and methods
data, respectively (level of significance p < 0.05). SPSS Software (v.24,
IBM, Armonk,NY) was used for all statistical analyses.
2.1. Study design

The Executive Committee of the ESSR approved this project in June 3. Results
2018. The Ethical Committee approval was not necessary since patients
were not involved. Seventy-three participants started the survey but one did not reply to
The survey has been structured into three sections: demographics any question. Therefore, the answers of 72 respondents (4% of the ESSR
Members), presumably only one from each workplace, were used for the

Fig. 1. Histogram showing the number of participants to the survey per country.

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C. Giraudo et al. European Journal of Radiology 136 (2021) 109533

Table 1
Closed-ended questions and frequencies of the answers about the application of WB-MRI for adults.
Closed-ended questions Answers to the closed-ended questions

Overall Subdivision of the answers according to the


answers workplace

Academic Private Public P*

n = 72 n=36 n=21 n=15


9/36 8/21 1/15
0 18 (25%)
(25%) (38.1%) (6.7%)
17 10/36 3/21 4/15
<20
(23.6%) (27.8%) (14.3%) (26.7%)
How many WBMRI for inflammatory diseases are performed per year in 15 10/36 2/21 3/15 0.196
20-49
your Center? (20.8%) (27.8%) (9.5%) (20%)
4/36 3/15
50-100 7 (9.8%) 0/21 (0%)
(11.1%) (20%)
15 3/36 8/21 4/15
>100
(20.8%) (8.3%) (38.1%) (26.7%)
n=61 n= 28 n=18 n=15
1/28 7/18 3/15
<1.5 T 11 (18%)
(3.6%) (38.9%) (20%)
What is the field strength of the MR that you use for WBMRI for
34 17/28 10/18 7/15 0.005
musculoskeletal inflammatory diseases? 1.5 T
(55.8%) (60.7%) (55.6%) (46.7%)
16 10/28 1/18 5/15
3T
(26.2%) (35.7%) (5.6%) (33.3%)
n=63 n = 30 n=18 n=15
4/30 9/18 4/15
GE 17 (27%)
(13.3%) (50%) (26.7%)
11 6/30 1/18 4/15
What is the vendor of the MR that you use for WBMRI for Philips
(17.5%) (20%) (5.6%) (26.7%) 0.027
musculoskeletal inflammatory diseases?
35 20/30 8/18 7/15
Siemens
(55.5%) (66.7%) (44.4%) (46.7%)
Toshiba 0 0/30 (0%) 0/18 (0%) 0/15 (0%)
Others 0 0/30 (0%) 0/18 (0%) 0/15 (0%)

n=58 n=28 n=15 n=15


Any myositis but idiopathic and 10 7/28 2/15 1/15
associated with overlap syndromesa (17.2%) (25%) (13.3%) (6.7%)
Idiopathic inflammatory 13 9/28 2/15 2/15
myopathiesb (22.4%) (32.1%) (13.3%) (13.3%)
What is the most common inflammatory clinical indication for WBMRI 3/28 6/15 3/15
SAPHO 8 (13.4%) 0.243
in adults in your Center? (10.7%) (40%) (20%)
4/28 1/15 3/15
Other rheumatic diseasec 3 (5.2%)
(14.3%) (6.7%) (20%)
Unspecific clinical signs of an 12 1/28 1/15 1/15
inflammatory disease (20.7%) (3.6%) (6.7%) (6.7%)
12 4/28 3/15 5/15
Rheumatoid Arthritis
(20.7%) (14.3%) (20%) (33.3%)
n= 63 n = 30 n=18 n=15
d 19 12/30 2/18 5/15
Mapping of abnormalities
(30.1%) (40%) (11.1%) (33.3%)
30 10/30 12/18 8/15
Diagnosis
(47.6%) (33.3%) (66.7%) (53.3%)
What do you mainly use WBMRI for? 3/30 0.328
Biopsies 3 (4.8%) 0/18 (0%) 0/15 (0%)
(10%)
1/30 2/18
Research 3 (4.8%) 0/15 (0%)
(3.3%) (11.1%)
4/30 2/18 2/15
Follow-upe 8 (12.7%)
(13.3%) (11.1%) (13.3%)
n = 61 n = 28 n=19 n=14
1/19
0 1 (1.6%) 0/28 (0%) 0/14 (0%)
(5.3%)
14 7/28 4/19 3/14
<25
(22.9%) (25%) (21.1%) (21.4%)
In how many cases did the WBMRI findings provide crucial information 12 7/28 2/19 3/14
25− 49
changing the clinical management (e.g., different diagnosis, (19.7%) (25%) (10.5%) (21.4%) 0.547
therapeutic change) of the patients? 14 6/28 7/19 1/14
50− 75
(22.9%) (21.4%) (36.8%) (7.1%)
2/28 1/19
>75 3 (5%) 0/14 (0%)
(7.1%) (5.3%)
17 6/28 4/19 7/14
I don’t know the clinical data
(27.9%) (21.4%) (21.1%) (50%)
n=60 n=28 n=17 n=15
31 17/28 10/17 4/15
Do you ever recommend local (i.e., single joint/single anatomical area) Yes
(51.7%) (60.7%) (58.8%) (26.7%) 0.081
MRI after WBMRI to confirm your findings?
29 11/28 7/17 11/15
No9
(48.3%) (39.3%) (41.2%) (73.3%)
(continued on next page)

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Table 1 (continued )
Closed-ended questions Answers to the closed-ended questions

Overall Subdivision of the answers according to the


answers workplace

Academic Private Public P*

n= 31 n=17 n=10 n=4


4/17 2/10
0 6 (19.3%) 0/4 (0%)
(23.5%) (20%)
8/17 4/10
<25 13 (42%) 1/4 (25%)
If you replied yes to the previous question, in how many cases was the (47.1%) (40%)
0.267
WBMRI positive diagnosis NOT confirmed at local MRI? 5/17 1/10
25− 49 9 (29%) 3/4 (75%)
(29.4%) (10%)
3/10
50− 75 3 (9.7%) 0/17 (0%) 0/4 (0%)
(30%)
>75 0 (0%) 0/17 (0%) 0/10 (0%) 0/4 (0%)
n=25 n=13 n=9 n=3
Inappropriate sequences 0 (0%) 0/13 (0%) 0/9 (0%) 0/3 (0%)
3/13 3/9
Inappropriate scan planes 6 (24%) 0/3 (0%)
(23.1%) (33.3%)
f 2/13 1/9 1/3
Technical issues 4 (16%)
If your previous answer was above 0%, do you have any explanation for (15.4%) (11.1%) (33.3%)
0.641
that? 3/13 1/9
Very small lesions 4 (16%) 0/3 (0%)
(23.1%) (11.1%)
3/9 1/3
Other 4 (16%) 0/13 (0%)
(33.3%) (33.3%)
5/13 1/9 1/3
I don’t know 7 (28%)
(38.5%) (11.1%) (33.3%)
n=61 n = 30 n=17 n=14
Do you apply the WBMRI protocol recommended by the Arthritis 31 10/30 12/17 9/14
Yes
Subcommittee of the ESSR# for adults with musculoskeletal (50.8%) (33.3%) (70.6%) (64.3%) 0.025
inflammatory diseases? 30 20/30 5/17 5/14
No
(49.2%) (66.7%) (29.4%) (35.7%)
n=57 n=28 n=16 n=13
24 9/28 10/16 5/13
Yes
Is DWI part of your protocol? (42.1%) (32.1%) (62.5%) (38.5%) 0.139
33 19/28 6/16 8/13
No
(57.9%) (67.9%) (37.5%) (61.5%)
n=57 n=28 n=16 n=13
24 10/28 9/16 5/13
Yes
Is DIXON part of your protocol? (42.1%) (35.7%) (56.3%) (38.5%) 0.369
33 18/28 7/16 8/13
No
(57.9%) (64.3%) (43.8%) (61.5%)
n=56 n=29 n =16 n =11
Do you refer to any other (i.e., other than the Guidelines of the Arthritis 4/29 1/16 2/11
Yes 7 (12.5%)
Subcommittee of the ESSR) Guidelines/Recommendation for (13.8%) (6.3%) (18.2%) 0.625
preparing the protocol? 49 25/29 15/16 9/11
No
(87.5%) (86.2%) (93.8%) (81.8%)
n=54 n=27 n=15 n=12
7/27 9/15 4/12
Yes 20 (37%)
Do you apply the same WBMRI protocol for oncologic imaging? (25.9-%) (60%) (33.3%) 0.087
20/27 6/15 8/12
No 34 (63%)
(74.1%) (40%) (66.7%)
n=56 n=28 n=16 n=12
32 21/28 6/16 5/12
0
(57.1%) (75%) (37.5%) (41.7%)
11 3/28 4/16 4/12
<25
(19.7%) (10.7%) (25%) (33.3%)
In how many cases do you apply contrast medium for WBMRI for
2/28 2/16 2/12 0.040
musculoskeletal inflammatory diseases? 25− 49 6 (10.7%)
(7.1%) (12.5%) (16.7%)
2/16 1/12
50− 75 3 (5.4%) 0/28 (0%)
(12.5%) (8.3%)
2/28 2/16
>75 4 (7.1%) 0/12 (0%)
(7.1%) (12.5%)
n = 40 n =17 n =13 n =10
10/17 6/13 4/10
0 20 (50%)
(58.8%) (46.2%) (40%)
5/17 1/13 4/10
<25 10 (25%)
(29.4%) (7.7%) (40%)
In how many cases did the contrast medium turn out to be essential to
1/13 0.503
reach the correct diagnosis? 25− 49 1 (2.5%) 0/17 (0%) 0/10 (0%)
(7.7%)
4/13 2/10
50− 75 6 (15%) 0/17 (0%)
(30.8%) (20%)
2/17 1/13
>75 3 (7.5%) 0/10 (0%)
(11.8%) (7.7%)
In your Center, are only radiologists with expertise in musculoskeletal n=57 n=28 n=18 n=11
0.239
radiology reporting WBMRI for inflammatory disease? Yes 41 (72%)
(continued on next page)

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Table 1 (continued )
Closed-ended questions Answers to the closed-ended questions

Overall Subdivision of the answers according to the


answers workplace

Academic Private Public P*

23/28 11/18 7/11


(82.1%) (61.1%) (63.6%)
No 16 (28%) 5/28 7/18 4/11
(17.9%) (38.9%) (36.4%)
n=57 n=28 n=17 n=12
Do you discuss the cases of patients undergoing WBMRI for 42 24/28 11/17 7/12
Yes
musculoskeletal inflammatory diseases with the clinicians in (73.7%) (85.7%) (64.7%) (58.3%) 0.119
multidisciplinary meetings? 15 4/28 6/17 5/12
No
(26.3%) (14.3%) (35.3%) (41.7%)
n=54 n =28 n =16 n =10
Qualitativeg;Semiquantitativeh ; 11 5/28 5/16 1/10
Quantitativei (20.4%) (17.9%) (31.3%) (10%)
24 14/28 5/16 5/10
Qualitativeg
(44.4%) (50%) (31.3%) (50%)
Which type of information do you include in your WBMRI report for
13 7/28 3/16 3/10
musculoskeletal inflammatory diseases? Qualitativeg;Semiquantitative h 0.296
(24.1%) (25%) (18.8%) (30%)
3/16 1/10
Semiquantitativeh 4 (7.4%) 0/28 (0%)
(18.8%) (10%)
2/28
Quantitativei 2 (3.7%) 0/16 (0%) 0/10 (0%)
(7.1%)
n=56 n =27 n =17 n =12
3/27 1/17 1/12
Yes 5 (9%)
Do you apply any scoring system? (11.1%) (5.9%) (8.3%)
0.836
24/27 16/17 11/12
No 51 (91%)
(88.9%) (94.1%) (91.7%)
n=58 n =28 n =18 n =12
8/28 2/18 1/12 (8.3-
Is your Center directly involved in research about WBMRI for Yes 11 (19%)
(28.6%) (11.1-%) %)
inflammatory diseases also beyond the musculoskeletal system? 0.193
20/28 16/18 11/12
No 47 (81%)
(71.4%) (88.9%) (91.7%)

n = number of respondents; *Comparisons among the three workplace environments were performed using the Chi-squared and the Kruskal-Wallis test for nominal and
ordinal data, respectively (applied level of significance, p < 0.05); #(coronal T1w, coronal T2-FS or STIR/TIRM and sagittal STIR/TIRM and/or T1w of the whole
spine).
SAPHO = synovitis–acne–pustulosis–hyperostosis–osteitis;
a
e.g., viral, drug-induced, paraneoplastic myositis; b dermatomyositis and polymyositis; c e.g., Sjogren, systemic lupus erythematosus; dpatients with known diagnosis;
e
assessment of treatment response; fe.g., low field strength, low signal to noise ratio; ge.g., pattern and extension of the lesions; h e.g., grading of the muscle lesions; I e.
g., dynamic-contrast-enhanced MRI kinetic parameters, ADC (apparent diffusion coefficient) values.

analyses. Electrics (27%), which is mostly applied in private practice (p = 0.027).


The most frequent indications of WB-MRI were IIM and any other
form of myositis (overall 39.7% of the respondents) followed by rheu­
3.1. Demographics
matoid arthritis (RA) and unspecific signs of inflammatory diseases
(20.1%,each). WB-MRI is considered of high value for myositis in gen­
Participants’ mean age was 40.9 ± 8.8 years and the average of
eral (Fig. 2A).
working experience was 10.4 ± 7.9 years. Sixty-two (87.1%) of the re­
WB-MRI is mainly used at diagnosis (47.6%), for mapping abnor­
spondents were from European countries, four from the United States
malities in patients with known diagnosis (30.1%), whereas it is less
(5.7%), two from Australia (2.8%), and one from South Korea (1.4%).
often used during follow-up (12.7%).
Italy provided the highest number of respondents (18.6%) (Fig. 1).
One-third of the respondents (27.9%) considered WB-MRI’s findings
as crucial for the clinical management in most of the examined cases
3.2. Adults (>50% of the cases).
Region-specific MRI following WB-MRI was considered useful for
The answers to the closed-ended survey questions regarding adult 51.7% of the participants, and only 9.7% of the respondents reported
patients are summarized in Table 1. that these second MR examinations did not confirm the WB-MRI findings
in most of the examined patients (>75).
3.2.1. MR scanners and clinical indications
Around thirty percent (30.6%) of the respondents performed at least 3.2.2. Protocols and sequences
50 WB-MRI exams per year for adults. Considering the limitations of WB-MRI, differences between whole
1.5 T MR magnets were most commonly used (55.8%), especially in body and local MR imaging were attributed to inappropriate scan planes
the academic environment (60.7%), followed by high-field MR (3 T) (24%), technical issues such as low field strength, low SNR, or lesions’
(p < 0.005). Siemens turned out to be the most common vendor size (16%, each);28% of the respondents declared that they did not
(55.5%), especially in academic workplaces, followed by General

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Fig. 2. Pie-charts representing the distribution of the answers to the open questions regarding the diseases for which WB-MRI is considered highly valuable and those
for which contrast medium is applied (a and c for adults and b and d for children).

using such guidelines, applied protocols based on the most updated


Table 2
literature, disease-tailored, and the ESTHER trial protocol [23].
Replies to the open question: “If you do not apply the WBMRI protocol recom­
Most of the respondents (63%) did not use the same protocol for
mended by the Arthritis Subcommittee of the European Society of Musculo­
rheumatologic and oncologic imaging.
skeletal Radiology, which other sequences/planes do you use and for which
areas?” for adults and pediatric patients. STIR and T1w were the most frequently applied sequences (Table 2)
and 42.1% of the respondents included DWI and DIXON. Contrast me­
Answers Adults Children
dium was rarely used (57.1% of the respondents never apply it) espe­
(n) (n)
cially by academics (p = 0.04). Gadolinium was mainly applied for RA
axial T2 DIXON 3
and myositis (Fig. 2C). The selection of scan planes was heterogeneous
coronal and axial T2 DIXON 1 2
axial T1 and T2 DIXON 1 1 (Table 2).
DWI only* 1 1
DWI and axial T2 focused on affected area 1 3.2.3. Reports, research, and work environment
DIXON and DWI* 2 WB-MRI was mainly performed and reported by musculoskeletal
axial and coronal T1, STIR and DWI 1
coronal and sagittal STIR 2 2
radiologists (72%) and the cases were typically discussed with the
coronal and axial STIR 1 referring clinicians in multidisciplinary meetings (73.7%).
coronal STIR 1 In the report, a qualitative approach, describing the pattern and
coronal and axial T1 and STIR 1 extension of the lesions (44.4%), followed by a combined semi­
coronal T1 and STIR 1
quantitative and qualitative approach (24.1%) was mostly used.
coronal T1 and STIR and sagittal STIR of the spine 1
coronal T1 and T1 contrast enhanced fat saturated 1 1 Only a minority (8.9%) of the respondents declared to rely on scoring
coronal T1 and STIR and sagittal T1 of the spine and DWI 1 systems (i.e.,in-house scoring system, scale for muscle assessment,
coronal T1 and STIR and axial STIR 1 Lecouvet scoring system for ankylosing spondylitis, and Spondyloar­
coronal STIR, sagittal STIR and T1 of the spine and 1 thritis Research Consortium of Canada score for spondyloarthritis) [18,
oblique coronal STIR of the sacroiliac joint
24,25].
disease specific protocols 1
Finally, only 18.9% of the respondents were involved in research
*
planes were not specified; STIR: short-tau inversion recovery sequence; DWI: activities. The most frequent research fields were RA (four respondents)
diffusion weighted imaging. followed by spondyloarthritis (three respondents), systemic sclerosis,
JIA, synovitis-acne-pustulosis-hyperostosis-osteitis (SAPHO), CRMO,
know the reason of such disagreement. and myositis (one respondent each).
In terms of WB-MRI protocol, 51% of the participants, especially Comparing the three work environments, no additional statistically
radiologists working in private practice (p = 0.025), referred to the significant differences were observed beside the above-mentioned
guidelines of the Arthritis Subcommittee of the ESSR. Participants not (p > 0.05,each).

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Table 3
Closed-ended questions and frequencies of the answers about the application of WB-MRI for children.
Closed-ended questions Answers to the closed-ended questions

Subdivision of the answers according to the


Overall workplace
answers
Academic Private Public P*

n=65 n=33 n=20 n=12


31 12/33 13/20 6/12
0
(47.8%) (36.4%) (65%) (50%)
17 10/33 3/12
<20 4/20 (20%)
(26.1%) (30.3%) (25%)
How many pediatric WBMRI for musculoskeletal inflammatory diseases
6/33 2/12 0.163
are performed per year in your Center? 20-49 9 (13.9%) 1/20 (5%)
(18.2%) (16.7%)
3/33 1/12
50-100 4 (6.1%) 0/20 (0%)
(9.1%) (8.3%)
2/33 0/12
>100 4 (6.1%) 2/20 (10%)
(6.1%) (0%)
n=61 n= 28 n= 18 n=15
1/28 7/18 3/15
<1.5 T = 11 11 (18%)
(3.6%) (38.9%) (20%)
What is the field strength of the MR that you use for WBMRI for pediatric
34 17/28 10/18 7/15 0.005
musculoskeletal inflammatory diseases? 1.5 T = 34
(55.8%) (60.7%) (55.6%) (46.7%)
16 10/28 1/18 5/15
3 T = 16
(26.2%) (35.7%) (5.6%) (33.3%)
n=63 n = 30 n =18 n =15
4/30 4/15
GE 17 (27%) 9/18 (50%)
(13.3%) (26.7%)
11 6/30 1/18 4/15
Philips
(17.5%) (20%) (5.6%) (26.7%)
What is the vendor of the MR that you use for WBMRI for musculoskeletal
35 20/30 8/18 7/15 0.027
pediatric inflammatory diseases? Siemens
(35.5%) (66.7%) (44.4%) (46.7%)
0/15
Toshiba 0 (0%) 0/30 (0%) 0/18 (0%)
(0%)
0/15
Others 0 (0%) 0/30 (0%) 0/18 (0%)
(0%)
n=39 n=23 n=7 n=9
Any myositis but idiopathic and
1/23 2/ 1/9
associated with overlap 3 (7.7%)
(4.3%) 7 = 13.3% (11.1%)
syndromesa
Idiopathic inflammatory 3/23 1/7 1/9
5 (12.8%)
myopathies b (13%) (14.3%) (11.1%)
19 14/23 1/7 4/9
CRMO
What is the most common inflammatory clinical indication for pediatric (48.7%) (60.9%) (14.3%) (44.4%)
0.013
WBMRI in your Center? 1/23 1/9
Overlap syndromes 2 (5.1%) 0/7 (0%)
(4.3%) (11.1%)
1/23 3/7 (42/
Other rheumatic diseasec 4 (10.3%) 0/9 (0%)
(4.3%) 9%)
2/23
JIA 2 (5.1%) 0/7 (0%) 0/9 (0%)
(8.7%)
Unspecific clinical signs of an 1/23 1/7 2/9
4 (10.3%)
inflammatory disease (4.3%) (14.3%) (22.2%)
n = 41 n=24 n =9 n =8
5/24 1/9 1/8
Mapping of abnormalitiesd 7 (17.1%)
(20.8%) (11.1%) (12.5%)
30 18/24 6/9 6/8
Diagnosis
In pediatric patients, what do you mainly use WBMRI for? (73.2%) (7%) (66.7%) (75%) 0.369
Biopsies 0 (0%) 0/24 (0%) 0/9 (0%) 0/8 (0%)
Research 0 (0%) 0/24 (0%) 0/9 (0%) 0/8 (0%)
1/24 2/9 1/8
Follow-up e 4 (9.7%)
(4.2%) (22.2%) (12.5%)
n=37 n= 22 n=7 n=8
1/22 2/7
0 3 (8.1%) 0/8 (0%)
(4.5%) (28.6%)
7/22 1/7 1/8
<25 9 (24.3%)
(31.8%) (14.3%) (12.5%)
In how many cases did the WBMRI findings provide crucial information 8/22 1/7 1/8
25− 49 10 (27%)
changing the clinical management (e.g., different diagnosis, (36.4%) (14.3%) (12.5%) 0.032
therapeutic change) of the pediatric patients? 4/22 1/7 1/8
50− 75 6 (16.2%)
(18.2%) (14.3%) (12.5%)
2/22 1/7 1/8
>75 4 (10.9%)
(9.1%) (14.3%) (12.5%)
1/7 4/8
I don’t know the clinical data 5 (13.5%) 0/22 (0%)
(14.3%) (50%)
n=37 n=22 n=6 n=9
In pediatric patients, do you ever recommend local (i.e., single joint/
13 9/22 2/6 2/9 0.610
single anatomical area) MRI after WBMRI to confirm your findings? Yes
(35.1%) (40.9%) (33.3%) (22.2%)
(continued on next page)

7
C. Giraudo et al. European Journal of Radiology 136 (2021) 109533

Table 3 (continued )
Closed-ended questions Answers to the closed-ended questions

Subdivision of the answers according to the


Overall workplace
answers
Academic Private Public P*

24 13/22 4/6 7/9


No
(64.9%) (59.1%) (66.7%) (77.8%)
n=17 n=10 n=4 n=3
2/10
0=3 3 (17.6%) 1/4 (25%) 0/3 (0%)
(20%)
5/10 2/3
If you replied yes to the previous question, in how many cases was the <25 = 7 7 (41.2%) 0/4 (0%)
(50%) (66.7%) 0.334
WBMRI positive diagnosis NOT confirmed at local MRI?
3/10 1/3
25− 49 = 5 5 (29.4%) 1/4 (25%)
(30%) (33.3%)
50− 75 = 1 1 (5.9%) 0/10 (0%) 1/4 (25%) 0/3 (0%)
>75 = 1 1 (5.9%) 0/10 (0%) 0/4 (0%) 0/3 (0%)
n=13 n=7 n=3 n=3
Inappropriate sequences 0 (0%) 0/7 (0%) 0/3 (0%) 0/3 (0%)
1/7
Inappropriate scan planes 1 (7.6%) 0/3 (0%) 0/3 (0%)
(14.3%)
3/7 2/3 2/3
Technical issuesf 5 (38.4%)
If your previous answer was above 0%, do you have any explanation for (42.9%) (66.7%) (66.7%)
0.411
that? 2/7 1/3
Very small lesions 4 (31%) 0/3 (0%)
(28.6%) (33.3%)
1/3
Other 2 (15.3%) 0/7 (0%) 0/3 (0%)
(33.3%)
1/7
I don’t know 1 (7.6%) 0/3 (0%) 0/3 (0%)
(14.3%)
n=39 n =23 n =8 n =8
Do you apply the WBMRI protocol recommended by the Arthritis
20 10/23 5/8 5/8
Subcommittee of the ESSR (coronal T1w, coronal T2-FS or STIR/TIRM Yes
(51.3%) (43.5%) (62.5%) (62.5%) 0.505
and sagittal STIR/TIRM and/or T1w of the whole spine) for pediatric
19 13/23 3/8 3/8
patients with musculoskeletal inflammatory diseases? No
(48.7%) (56.5%) (37.5%) (37.5%)
n = 40 n=24 n=9 n=7
5/24 7/9 3/9
Yes 15 (37.5)
Is DWI part of your protocol? (20.8%) (77.8%) (42.9%) 0.010
25 19/24 2/9 4/9
No
(62.5%) (79.2%) (22.2%) (57.1%)
n=38 n=23 n=9 n=6
15 7/23 6/9 2/6
Yes
Is DIXON part of your protocol? (39.5%) (30.4%) (66.7%) (33.3%) 0.160
23 16/23 3/9 4/6
No
(60.5%) (69.6%) (33.3%) (66.7%)
n=37 n =22 n =9 n =6
Do you refer to any other (i.e., other than the Guidelines of the Arthritis 1/22 1/9
Yes 2 (55%) 0/6 (0%)
Subcommittee of the ESSR) Guidelines/Recommendation for preparing (4.5%) (11.1%) 0.623
the pediatric WBMRI protocol? 21/22 8/9 6/6
No 35 (95%)
(95.5%) (88.9%) (100%)
n=36 n =22 n =7 n =7
11 5/22 3/7 3/7
Yes
Do you apply the same WBMRI protocol for pediatric oncologic imaging? (30.5%) (22.7%) (42.9%) (42.9%) 0.442
25 17/22 4/7 4/7
No
(69.5%) (77.3%) (57.1%) (57.1%)
n=37 n =23 n =7 n =7
25 17/23 4/7 4/7
0
(67.6%) (73.9%) (57.1%) (57.1%)
3/23 1/7 1/7
<25 5 (13.5%)
(13%) (14.3%) (14.3%)
In how many cases do you apply contrast medium for WBMRI for
1/7 1/7 0.582
pediatric musculoskeletal inflammatory diseases? 25− 49 2 (5.4%) 0/23 (0%)
(14.3%) (14.3%)
2/23 1/7
50− 75 3 (8.1%) 0/7 (0%)
(8.7%) (14.3%)
1/23 1/7
>75 2 (5.4%) 0/7 (0%)
(4.3%) (14.3%)
n = 28 n =16 n =6 n =6
16 10/16 3/6
0 3/6 (50%)
(57.1%) (62.5%) (50%)
3/16 1/6 1/6
<25 5 (17.9%)
(18.8%) (16.7%) (16.7%)
In how many cases did the contrast medium turn out to be essential to
1/6 1/6 0.808
reach the correct diagnosis? 25− 49 2 (7.1%) 0/16 (0%)
(16.7%) (16.7%)
2/16 1/6
50− 75 3 (10.8%) 0/6 (0%)
(12.5%) (16.7%)
1/16 1/6
>75 2 (7.1%) 0/6 (0%)
(6.3%) (16.7%)
n=37 n=22 n=9 n=6 0.032
(continued on next page)

8
C. Giraudo et al. European Journal of Radiology 136 (2021) 109533

Table 3 (continued )
Closed-ended questions Answers to the closed-ended questions

Subdivision of the answers according to the


Overall workplace
answers
Academic Private Public P*

25 18/22 3/9 4/6


In your Center, are only radiologists with expertise in pediatric radiology Yes
(67.6%) (81.8%) (33.3%) (66.7%)
and/or musculoskeletal radiology reporting WBMRI for inflammatory
12 4/22 6/9 2/6
disease? No
(32.4%) (18.2%) (66.7%) (33.3%)
n=37 n =22 n =8 n =7
Do you discuss the cases of pediatric patients undergoing WBMRI for 31 21/2 5/8 5/7
Yes
musculoskeletal inflammatory diseases with the clinicians in (83.8%) (95.5%) (62.5%) (71.4%) 0.059
multidisciplinary meetings? 1/22 3/8 2/7
No 6 (16.2%)
(4.5%) (37.5%) (28.6%)
n=38 n =23 n =9 n =6
Qualitativeg;Semiquantitative h; 2/23 3/9
5 (13.2%) 0/6 (0%)
Quantitativei (8.7%) (33.3%)
g 18 11/23 4/9 3/6
Qualitative
(47.3%) (47.8%) (44.4%) (50%)
Which type of information do you include in your WBMRI report for
10 7/23 3/6 0.141
pediatric musculoskeletal inflammatory diseases? Qualitative g;Semiquantitativeh 0/9 (0%)
(26.3%) (30.4%) (50%)
1/23 2/9
Semiquantitativeh 3 (7.9%) 0/6 (0%)
(4.3%) (22.2%)
2/23
Quantitative i 2 (5.3%) 0/9 (0%) 0/6 (0%)
(8.7%)
n=36 n =21 n =8 n =7
1/8
Yes 1 (2.8%) 0/21 (0%) 0/7 (0%)
Do you apply any scoring system? (12.5%) 0.165
35 21/21 7/8 7/7
No
(97.2%) (100%) (87.5%) (100%)
n=35 n =21 n =6 n =8
6/21 1/6 1/8
Is your Center directly involved in research about WBMRI for pediatric Yes 8 (22.9%)
(28.6%) (16.7%) (12.5%) 0.605
inflammatory diseases also beyond the musculoskeletal system?
27 15/21 5/6 7/8
No
(77.1%) (71.4%) (83.3%) (87.5%)

n = number of respondents; *Comparisons among the three workplace environments were performed using the Chi-squared and the Kruskal-Wallis test for nominal and
ordinal data, respectively (applied level of significance, p < 0.05); #(coronal T1w, coronal T2-FS or STIR/TIRM and sagittal STIR/TIRM and/or T1w of the whole
spine).
CRMO = chronic recurrent multifocal osteomyelitis; JIA = juvenile idiopathic arthritis.
a
e.g., viral, drug-induced, paraneoplastic myositis; b juvenile dermatomyositis and polymyositis; c e.g., systemic lupus erythematosus, scleroderma; ; dpatients with
known diagnosis; eassessment of treatment response; fe.g., low field strength, low signal to noise ratio; ge.g., pattern and extension of the lesions; h e.g., grading of the
muscle lesions; I e.g., dynamic-contrast-enhanced MRI kinetic parameters, ADC values.; ; ge.g., pattern and extension of the lesions; h e.g., grading of the muscle lesions;
I
e.g., dynamic-contrast-enhanced MRI kinetic parameters, ADC values.

3.3. Pediatrics (38.5%) and to small lesions’ size (31%).

The answers to the closed-ended questions of the survey section 3.3.2. Protocols and sequences
regarding children are summarized in Table 3. The protocol of the Arthritis Subcommittee of the ESSR was used by
half of the respondents (51.3%); only two referred to other guidelines. In
3.3.1. MR scanners and clinical indications particular, one respondent applied disease specific recommendations
The results regarding MR field strengths and vendors are the same as and another one used a protocol including coronal T1w, STIR, DWI, and
for adults (see section above). sagittal T1w of the spine without mentioning if it was part of specific
Around twelve percent (12.3%) of the respondents perform at least guidelines. Only 30% applied the same protocol as for oncological
50 WBMRI exams per year for children. imaging.
The most frequent pediatric indication of WB-MRI was CRMO DWI and DIXON were used by 37.5% and 39.5% of the participants.
(48.7%) especially in academic centers (p = 0.013) (Fig. 2B). Regarding DWI, it was mostly applied in private practice (p = 0.01).
As for adults, WB-MRI was mainly used for diagnosis (73.2%). Only a few participants used contrast medium in most of their cases
Twenty-seven percent of the respondents declared that WB-MRI pro­ (>50% of the cases) (15%) considering it useful for JIA, myositis,
vides crucial information for the clinical management in more than half CRMO; one participant declared to use it in all cases (Fig. 2D).
of the examined population (>50% of the cases). Region-specific MR
scans were considered necessary after WB-MRI by 35% of the re­ 3.3.3. Reports, research, and work environment
spondents. Overall for 59% of the respondents, in less than 25% of their WB-MRI was mainly reported by radiologists specialized in muscu­
patients, the WB-MRI positive diagnosis was not confirmed at local MRI. loskeletal and/or pediatric imaging (65.7%), especially in academic
Differences between whole-body and local MR imaging were mainly hospitals (p = 0.032); 84% of the respondents discussed the WB-MRI
attributed to technical issues such as low field-strength or low SNR findings with clinicians.

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C. Giraudo et al. European Journal of Radiology 136 (2021) 109533

A qualitative alone or a combined qualitative and semiquantitative


approach were mainly applied (47.4% and 26.3%, respectively). Only
one respondent declared to use a scoring system without mentioning
which one.
Twenty-three percent of the participants were involved in research
on WB-MRI mainly focused on CRMO, followed by myositis, JIA, sickle
cell disease, juvenile spondyloarthritis, and protocol optimization.

4. Discussion

There is a growing body of literature about WB-MRI, showing its high


accuracy and efficacy in various rheumatic diseases [16–22,26]. How­
ever, according to the current survey, its application in routine practice
is still limited, independently of the workplace environment. In our
study, despite the collection of geographical information from the re­
spondents, we could not evaluate if the little use of WB-MRI is somehow
associated with the limited availability of MRI scanners in some coun­
tries [27]. Further studies including this type of data should be promoted
in the future.
Regarding the type of disease, though robust evidence is available
especially for RA, psoriatic arthritis, and spondyloarthritis, interest­
ingly, among our respondents, WB-MRI is mainly applied for IIM [16,
17] (Fig. 3). This result might be related to the respondents’ areas of
expertise since they also declared to perform most of their research ac­
tivity in that field. Moreover, myositis does not require additional plans
and/or sequence and represents one of the historical indications of
WB-MRI for adults and children [28,29] (Fig. 4).
In children, CRMO was the most frequent indication and this result is
consistent with the literature [22,30,31]. Indeed, it has been demon­
strated that WB-MRI is superior to other imaging modalities for a precise
assessment of CRMO’s features like symmetry and multifocality and it
may be considered the first line imaging modality [22,30–32] (Fig. 5).
Our results are in line with those of the survey of Schooler et al., who,
exploring the overall use of WB-MRI in pediatric patients, showed that
CRMO was the second most frequent indication, after neurofibromatosis
[22].
It should not be overlooked that even rare disorders like systemic
sclerosis or systemic lupus erythematosus could benefit of a whole-body
approach [14]. However, overall, specific indications of WB-MRI in
research, trials, and routine practice still have to be precisely defined.
WB-MRI is certainly affected by some limitations which have also
been highlighted by our respondents. Usually, whole-body scans do not
allow high resolution images of single joints and sometimes additional
examinations of a single area have to be performed. Nevertheless, our
study indicates that these second line examinations are usually in line
with the WB-MRI findings. Thus, tailoring the WB-MRI protocol to pa­
tients’ disease (e.g., adding a scan of the hands to the WB-MRI protocol
in patients with RA or excluding a scan of the head in JIA) may avoid
multiple examinations afterwards.
Concerning the protocol, especially radiologists working in private
practice adhered to specific guidelines like the ones of the Arthritis
Subcommittee of the ESSR. The need of standardization might be related
to time pressure. In fact, the protocol mentioned above requires only
around half-an-hour.
The main applied sequences for WB-MRI are T1w and STIR while a
more heterogeneous approach emerged regarding the scanning plane.
Additionally to axial and coronal planes, some radiologists apply sagittal
or coronal oblique scans respectively for the spine or the sacroiliac joint,
Fig. 3. Coronal STIR WB-MRI image of a 35 years-old female affected by reflecting a need for disease-adapted protocols.
myositis, well demonstrating muscle edema in both legs (white arrows). In the debate about protocols’ optimization, despite the growing
evidence about WB-DWI and DIXON, their clinical application in the
rheumatological setting seems to be limited [18,19,33] (Fig. 6). We
assume that major constraints to DWI’s routinely use, although it
demonstrated, for instance, to outperform STIR in lesions’ detection and
to be an alternative to contrast medium in children with JIA, might be
attributed to the prolonged scanning time and the risk of artifacts [34,

10
C. Giraudo et al. European Journal of Radiology 136 (2021) 109533

Fig. 4. Coronal STIR WB-MRI of a six years-old boy affected by juvenile dermatomyositis, showing diffuse muscle edema affecting the paravertebral muscles, the
iliopsoas, and the muscles of the extremities (white arrows).

35]. Regarding DIXON, even if it has already shown a good performance comprising rheumatologists and pediatric radiologists, may provide
especially in the oncological field, its use is probably hampered by the additional insights and deliver a different perspective. It should also be
fact that many radiologists do not want to replace T1w and STIR and considered that the length of the survey may have discouraged the re­
using DIXON as additional sequence would be extremely time sponders. The survey was especially long because it included two main
consuming [36,37]. Further studies about fast-DIXON protocols may sections (i.e., adults and pediatrics). In the future, using two distinct and
increase its application [37]. shorter questionnaires may guarantee a higher participation. Despite
Gadolinium is rarely utilized and mainly recommended for RA by our these drawbacks, it should be highlighted that the current response rate
respondents. Some radiologists reported its use for myositis in adults, (4%) was very similar to the one of the survey of Schooler et al.(5%)
though it is not supported by the current literature. Contrast medium about pediatric WB-MRI demonstrating that WB-MRI is still a niche field
should be further questioned in children because of the recent evidence [22].
of tissues deposition and other methods and sequences promoted [38]. Second, since the questionnaire was on a voluntary base, the self-
In terms of reporting and image analyses, the interviewed commu­ selection bias causing a nonprobability sampling should be consid­
nity mainly provides qualitative information and just a few use scoring ered. However, the distribution of the survey via the ESSR guaranteed
systems. In particular, the SAPHO, the CRMO and the recent OMERACT that, as above-mentioned, radiologists working especially in the
scoring systems are not routinely applied [26,39–41]. Using such a musculoskeletal field participated, mitigating the impact of the bias.
standardized approach, possibly combined with quantitative measure­ Then, it might be seen as a limit that only DWI and DIXON were
ments at diagnosis and follow-up, should be encouraged since it may explicitly addressed, not directly mentioning other sequences like T1
increase our accuracy for the diagnosis and the treatment response. and T2 mapping. Nevertheless, this choice was based on the fact that
Some limitations of this study need to be underlined. these sequences have already been widely tested in WB-MRI protocols
First, the low response rate should be addressed. It could be partially for rheumatic diseases [18,19,21,33]. Moreover, the respondents had
due to the way of distribution. Probably the involvement of various the chance to reply to open questions about their research field and
Colleges of radiology and not only of the ESSR would have increased the provide additional comments including remarks about particular se­
participation but, focusing on inflammatory musculoskeletal diseases, quences or protocols.
we wanted to initially include experts in this field. A next project, In conclusion, despite the interest for WB-MRI and the recent

11
C. Giraudo et al. European Journal of Radiology 136 (2021) 109533

Fig. 5. Coronal and axial STIR of an eleven years-old girl with pain in multiple sites for several weeks affected by CRMO, demonstrating the numerous areas of bone
marrow edema in the scapulae, left iliac bone, tibiae, and thoracic spine (arrows in A and B).

evidence that it is a robust diagnostic tool for rheumatic inflammatory analysis, Writing - review & editing. Iwona Sudoł-Szopińska:
diseases, this technique is routinely applied only by a limited number of Conceptualization, Methodology, Writing - review & editing,
musculoskeletal radiologists. Elaboration of specific guidelines by in­ Supervision.
ternational working groups, including the newly proposed scoring sys­
tems and the most recent technical improvements, should further Declaration of Competing Interest
promote the use of WB-MRI in this field.
None of the Authors of the submitted manuscript “Whole-body
CRediT authorship contribution statement magnetic resonance imaging in inflammatory diseases: Where are we
now? Results of an International Survey by the European Society of
Chiara Giraudo: Conceptualization, Methodology, Writing - orig­ Musculoskeletal Radiology.” has any financial support or conflicts of
inal draft. Frederic E. Lecouvet: Methodology, Writing - review & interest related to the subject of the article to declare.
editing, Resources. Anne Cotten: Writing - review & editing, Method­ The manuscript has not been published or is considered for publi­
ology. Iris Eshed: Writing - review & editing, Resources. Lennart Jans: cation, elsewhere.
Writing - review & editing, Supervision. Anne Grethe Jurik: Method­ All authors have approved the manuscript and have significantly
ology, Writing - review & editing, Resources. Mario Maas: Methodol­ contributed to it.
ogy, Writing - review & editing, Resources. Michael Weber: Formal

12
C. Giraudo et al. European Journal of Radiology 136 (2021) 109533

Fig. 6. WB-MRI in a 43-years old male patient with ankylosing spondylitis with inflammatory pelvic pain. Coronal STIR (A) and DWI (inverted grey scale) (B)
showing involvement of the anterior part of the thoracic spine (arrowheads) and of the sacroiliac joint (arrows): the lesions are by far more evident on the DWI
sequence, due to the high contrast with the background.

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