Rheumatology International (2022) 42:1257–1264

https://doi.org/10.1007/s00296-021-05041-9
Rheumatology
INTERNATIONAL

IMAGING

Comparison of contrast‑enhanced MRI features of the (teno)synovium

in the wrist of patients with juvenile idiopathic arthritis and pediatric
controls
Jeffrey M. A. van der Krogt1 · F. Verkuil1,2 · E. Charlotte van Gulik1,2 · Robert Hemke1 ·
J. Merlijn van den Berg2 · Dieneke Schonenberg‑Meinema2 · Angelika Kindermann3 · Koert M. Dolman4 ·
Marc A. Benninga3 · Taco W. Kuijpers2 · Mario Maas1 · Charlotte M. Nusman1,2

Received: 26 August 2021 / Accepted: 26 October 2021 / Published online: 22 November 2021
© The Author(s) 2021

Abstract
To directly compare and describe the differences between juvenile idiopathic arthritis (JIA) patients and pediatric controls
regarding features of the synovial and tenosynovial membrane on contrast-enhanced magnetic resonance imaging (MRI) of
the wrist. T1-weighted contrast-enhanced MRI scans of 25 JIA patients with clinically active wrist arthritis and 25 children
without a history of joint complaints nor any clinical signs of joint inflammation were evaluated by two readers blinded to
clinical data. The synovium was scored at five anatomical sites based on thickening of the synovium (0–3 scale) and synovial
enhancement (0–2 scale). Thickening and/or enhancement of the tenosynovium was scored at four anatomical sites using a
0–3 scale. Significantly higher scores for synovial thickening (median 4 vs. 1, p < 0.001) and synovial enhancement (median
4 vs. 1, p < 0.001) are found in the wrist of JIA patients as compared to controls. JIA patients experienced the highest synovial
scores at the mid-/inter-carpal, 2nd –5th carpometacarpal, and radiocarpal joints. No significant difference in tenosynovial
scores is found between both groups (median 0 vs. 0, p = 0.220). This study highlights the higher synovial thickening/
enhancement scores on contrast-enhanced MRI of the wrist in JIA patients compared to pediatric controls. Tenosynovial
thickening and/or enhancement was rarely present in both groups. In JIA patients, synovial thickening and enhancement
were particularly present at three anatomical sites. These results substantially support rheumatologists and radiologists when
navigating through MRI of the wrist in search for JIA disease activity.

Keywords Juvenile idiopathic arthritis · Magnetic resonance imaging · Wrist

Introduction
* Charlotte M. Nusman
[email protected] Juvenile idiopathic arthritis (JIA) is typically characterized
1
by soft tissue inflammation, such as synovitis and tenosyno-
Department of Radiology and Nuclear Medicine, vitis [1]. At first presentation of JIA, disease activity in the
Amsterdam University Medical Centers (Amsterdam UMC),
Location AMC, University of Amsterdam, Meibergdreef 9, wrist is present in 23% of all patients [2]. Contrast-enhanced
1105 AZ Amsterdam, The Netherlands magnetic resonance imaging (MRI) is a helpful technique for
2
Department of Pediatric Immunology, Rheumatology diagnosing and grading soft tissue pathology [3].
and Infectious Diseases, Emma Children’s Hospital, To reliably determine JIA disease activity in the wrist
Amsterdam University Medical Centers (Amsterdam joint of children, contrast-enhanced MRI scores for the
UMC), University of Amsterdam, Meibergdreef 9, assessment of the synovium [4] and tenosynovium [5] in the
1105 AZ Amsterdam, The Netherlands
3
wrist of children have been developed. Recently, a study on
Department of Pediatric Gastroenterology and Nutrition, MRI findings in the wrist of children showed that mild (teno)
Emma Children’s Hospital, Amsterdam University Medical
Centers (Amsterdam UMC), University of Amsterdam, synovial enhancement and/or thickening can be considered
Meibergdreef 9, 1105 AZ Amsterdam, The Netherlands as normal [6]. Besides, a distribution pattern of preferred
4
Department of Pediatrics, OLVG Hospital, Location West, locations for disease activity in the JIA wrist has previ-
Jan Tooropstraat 164, 1061 AE Amsterdam, The Netherlands ously been established [7]. Direct comparison of the (teno)

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synovial MRI scores between JIA patients and pediatric con- MRI protocol
trols has not yet been done. This knowledge contributes to
a roadmap for the rheumatologist and radiologist to enable Clinically active JIA patients underwent an axial wrist
rapid and easy navigation through contrast-enhanced MRI T1-weighted MRI sequence with fat saturation (TR
of the wrist when assessing JIA disease activity. 400–750 ms, TE 10 ms; slice thickness 4 mm; field of view
The aim of this study is to directly compare and describe 150 × 150 mm, matrix 384 × 384) using a 1.0 T MRI scan-
the differences between JIA patients and pediatric controls ner (Panorama HFO, Philips Healthcare), after intravenous
regarding features of the synovial and tenosynovial mem- contrast agent administration (Gadovist, Bayer Schering
brane on contrast-enhanced MRI of the wrist. Second, the Pharma, Berlin, Germany, 1.0 mmol gadolinium/mL, dose
distribution pattern of contrast-enhanced MRI features of the 0.1 mmol/kg).
synovium and tenosynovium of the wrist is evaluated and Children from the control group initially underwent MR
compared between both groups. enterography using a 1.5 T MRI scanner (MAGNETOM
Avanto™, Siemens Medical Systems) after intrave-
nous contrast administration (Gadovist, Bayer Schering
Pharma, Berlin, Germany, 1.0 mmol gadolinium/mL,
Materials and methods dose 0.1 mmol/kg). Following a change of position for
correct placement of the wrist coil and without repeated
Clinically active JIA patients intravenous contrast agent administration, an axial con-
trast-enhanced MRI sequence with fat saturation (TR
JIA patients were selected from a multicenter prospective 400–750 ms, TE 10 ms; slice thickness 4 mm; field of
observational JIA patient database (May 2012–July 2013). view 150 × 150 mm, matrix 384 × 384) was obtained from
Since a prolonged time interval between intravenous con- the wrist. Precautionary measures were made to ensure
trast agent administration and image acquisition is known minimal time interval between intravenous contrast injec-
to increase synovial thickness upon contrast-enhanced MRI tion and image acquisition.
examination [8], only JIA patients of whom the time interval
from contrast fluid injection to the start of MRI examination
was under 20 min were selected. All JIA patients had clini- Image analysis
cal arthritis in the wrist examined. JIA disease activity was
scored by the referring pediatric rheumatologist using the General agreement on the scores and conformity on the
Juvenile Arthritis Disease Activity Score-10 (JADAS-10) appearance of hyper-intense structures were achieved dur-
[9]. In addition, clinical disease remission or inactivity was ing a preliminary calibration session (Fig. 1). After being
ruled out using the Wallace criteria [10]. blinded for clinical data, image sets of each participant
were scored by two musculoskeletal radiologists (12 and
25 years of experience in musculoskeletal radiology) by
Pediatric control group means of consensus. Two MRI features of the synovium
and one of the tenosynovium were evaluated according to
Because of ethical objections, it is not possible to undergo existing scoring methods [4, 5].
a MRI procedure nor administer intravenous contrast agent In accordance with the scoring method introduced by
to healthy children. Alternatively, children with suspected Damasio et al. [4], the synovium was assessed for two
or confirmed inflammatory bowel disease (IBD), who were features, namely thickening of the synovium and synovial
scheduled for IBD-related MR enterography with intra- enhancement. Effusion was out of the scope of this study,
venous contrast agent administration, were prospectively since no T2-weighted sequences were available. In the
included between July 2012 and March 2014. A similar current study, both synovial features were scored at five
approach was applied to a previous study on the comparison predefined anatomical sites: (1) carpometacarpal recess 1,
of enhancing synovial thickness in the knee upon contrast- (2) carpometacarpal joints 2–5, (3) radiocarpal, (4) distal
enhanced MRI between clinically active JIA patients and radioulnar, and (5) mid-/inter-carpal (Fig. 2a). First, the
pediatric controls [11]. Joint abnormalities, joint complaints degree of thickening of the synovium was scored (0: no
and joint inflammation were ruled out in these children by thickening, 1: mild thickening, 2: moderate thickening,
a research fellow following the pediatric Gait Arms Legs 3: severe thickening). An example of a contrast-enhanced
Spine (pGALS) screening method [12]. The research fel- MRI image of severe thickening in the wrist of a 17-year-
low was trained to perform examination and the screen- old female JIA patient is displayed in Figure 2b. Second,
ing method by a pediatric rheumatologist (25 years of the degree of synovial enhancement was scored (0: normal
experience).

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Fig. 1  Hyper-intense cartilage mimics synovial enhancement.

T1-weighted contrast-enhanced and fat-saturated MRI of a moder-
ately increased synovial enhancement in the wrist of a 15-year female
patient indicated by the arrows and b hyper-intense cartilage of the
wrist in a 10-year old female patient indicated by the arrow

synovial enhancement as compared to neighboring muscle,

(1) mildly increased synovial enhancement, (2) moderately
to severely increased synovial enhancement. An example
of a contrast-enhanced MRI image of severely increased
synovial enhancement in the wrist of a 9-year-old female
JIA patient is displayed in Figure 2c. Per individual child,
total scores of both synovial features were separately
obtained by summing the scores of each feature from all
five anatomical scoring sites, generating maximum achiev-
Fig. 2  a Anatomical scoring sites of the synovium. (I) First carpo-
able total scores of 15 for thickening of the synovium and metacarpal recess, (II) 2nd–5th carpometacarpal joints, (III) Radio-
10 for synovial enhancement. carpal joint, (IV) Distal radioulnar joint, (V) Mid-/inter-carpal joints.
In accordance with the scoring method introduced by Example of a contrast-enhanced MRI image of b severe synovial
Lambot et al. [5], the tenosynovium was assessed by a semi- thickening in the wrist of a 17-year-old female JIA patient, and (c)
severe synovial enhancement in the wrist of a 9-year-old female JIA
quantitative simultaneous evaluation of enhancement and patient
thickening of the tendon sheath (0: no enhancement and
no thickened synovial sheath, (1) enhancement and mildly
thickened synovial sheath, (2) enhancement and moderately Since the originally proposed scoring methods for the
to significantly thickened synovial sheath). The tenosyn- assessment of the (teno)synovium to which we refer in the
ovium was evaluated in both extensor and flexor tendons. current study proved intra-observer agreements sufficient
Extensor tendons (second, fourth, and sixth compartments) for clinical use [4, 5], participants of the current study were
were scored at the axial height of Lister’s tubercle, as illus- scored once, in consensus between both readers.
trated in Fig. 3a. Flexor tendons were scored as a bundle at
the axial height of the carpal tunnel, as illustrated in Fig. 3b. Statistical analysis
Per individual child, the total score for tenosynovial thicken-
ing and enhancement was obtained by summing the scores Based on a previous study comparing contrast-enhanced
from all four anatomical scoring sites, generating a maxi- MRI features of the (teno)synovium in the knee of JIA
mum achievable total score of 8. patients with pediatric controls [11], we made a sample size

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Table 1  Baseline clinical characteristics of study groups

Clinically active Control

JIA patients group
(n = 25) (n = 25)

No. (%) of female subjects 17 (68) 11 (44)

Age at MRI, years; mean (SD)* 13.2 (2.8) 14.9 (2.3)
Time interval from intravenous 10 (1) 11.50 (5)a
contrast to MRI wrist, minutes;
median (IQ-r)***
JADAS-10 (0–40), median (IQ-r) 7.5 (12) –
Diagnosis JIA, no. (%)
Oligo-articular persistent 5 (20) –
Oligo-articular extended 3 (12) –
Poly-articular RF- 11 (44) –
Poly-articular RF + 1 (4) –
Psoriatic arthritis 2 (8) –
Enthesitis related JIA 2 (8) –
Unclassified 1 (4) –
PCDAI, n = 18; mean (SD) – 23 (14)
PUCAI, n = 7; mean (SD) – 35 (16)
Diagnosis ­IBDb, no. (%)
Fig. 3  a Tenosynovium extensor tendon scoring compartments (II)
Crohn’s disease – 14 (56)
extensor carpi radialis longus/extensor carpi radialis brevis, (IV)
extensor indicis proprius/extensor digitorum communis, (VI) exten- Ulcerative colitis – 7 (28)
sor carpi ulnaris, (LT) Lister’s tubercle and (b) flexor tendon scoring No or other disorder – 4 (16)
compartment (s) scaphoid, (p) pisiform, (u) ulnar artery
Values are mean (standard deviation) for age, PCDAI and PUCAI.
Values are median (interquartile range) for time interval and JADAS-
calculation in nQuery based on comparing means with a 10
Mann–Whitney U test for continuous outcomes with the MRI magnetic resonance imaging, PCDAI Pediatric Crohn’s Disease
following numbers: alpha 0.05, 2-sided, power 80%, mean Activity Index, PUCAI Pediatric Ulcerative Colitis Activity Index,
of 0.92 in the control group, 2.92 in the JIA group and a IBD inflammatory bowel disease, JIA Juvenile idiopathic arthritis,
JADAS Juvenile Arthritis Disease Activity Score, RF rheumatoid fac-
common standard deviation of 2.329. This resulted in a num- tor
ber of 26 patients per study group, similar to our presented *p ≤ 0.05, ***p ≤ 0.001, a
n = 24, bfinal diagnosis
work. The Shapiro–Wilk test was used to test for normality
of the results within study groups. Descriptive statistics were
used to specify baseline characteristics in terms of number consent to participate and for publication was obtained
(percentage), mean [standard deviation (SD)], and median from all individuals included.
[interquartile range (IQ-r)]. Unpaired t tests were used to
examine differences in time interval from contrast fluid
injection to start MRI between the group of JIA patients
and the pediatric control group. Mann–Whitney U tests were Results
performed to analyze differences in age and (teno)synovial
scores between both groups. Statistical significance was Participant characteristics
defined as a p value < 0.05. These statistical analyses were
performed with the use of IBM SPSS Statistics, Version 26 Twenty-five clinically active JIA patients (68% female)
(IBM Corporation). and 25 children from the control group (44% female)
were included. On average, children from the control
Compliance with ethical standards group were significantly older (mean ± SD 14.9 ± 2.3 vs.
13.2 ± 2.8 years, p < 0.05) and had a significantly longer
The authors declare that there is no conflict of interest. time interval from intravenous contrast injection to image
This study has been conducted according to the World acquisition as compared to JIA patients (median ± IQ-r
Medical Association Declaration of Helsinki. Institutional 11.5 ± 5 vs. 10.0 ± 1 min, p < 0.001). Complete baseline
review board approval by the Medical Ethics Committee at characteristics of the children included are summarized
the XXX in XXX was obtained (XXX). Written informed in Table 1.

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Total scores of the synovium and tenosynovium

Within the group of clinically active JIA patients, both

the total synovial thickening score (median ± IQ-r 4 ± 3
vs. 1 ± 1, p < 0.001; Fig. 4a) as well as the total synovial
enhancement score (median ± IQ-r 4 ± 2 vs. 1 ± 1, p < 0.001;
Fig. 4b) appeared significantly higher as compared to the
control group. Regarding the total tenosynovial thickening
and/or enhancement score, no significant difference was
found between clinically active JIA patients and controls
(median ± IQ-r 0 ± 1 vs. 0 ± 1, p = 0.220; Fig. 4c).

JIA‑specific distribution pattern of (teno)synovial

features

To determine the JIA-specific distribution pattern of (teno)

synovial features in the wrist on contrast-enhanced MRI,
scores from all separate anatomical scoring sites were
compared between JIA patient and control groups. In com-
parison to pediatric controls, clinically active JIA patients
showed significantly higher scores of synovial thickening
at all five anatomical scoring sites (Fig. 5a). Regarding
synovial enhancement, scores were significantly increased
in JIA patients at the first carpometacarpal recess, 2nd–5th
carpometacarpal, mid-/inter-carpal and radiocarpal joints
(Fig. 5b). Further evaluation of the distribution pattern of
tenosynovial thickening and/or enhancement showed no sig-
nificant differences between both groups at any of the four
anatomical scoring sites (Fig. 5c).
A grayscale map has been created to visualize the differ-
ence in scores for both clinical features of synovium in the
wrist between JIA patient and control groups (Fig. 6). This
map indicates three anatomical scoring sites to be major
determinants for the difference in synovial scores between
JIA patients and controls, namely the mid-/inter-carpal, the
2nd–5th carpometacarpal, and the radiocarpal joints.

Discussion

This is the first study to directly compare contrast-enhanced

MRI features of the synovium and tenosynovium in the wrist
between clinically active JIA patients and pediatric controls.
Synovial thickening and -enhancement, was significantly
more present in JIA patients compared to pediatric con-
trols, in whom it was present in a low grade. Based on the
results of this study, the mid-/inter-carpal, carpometacarpal
2nd–5th, and radiocarpal joints are susceptible for develop-
Fig. 4  Differences in total synovial and total tenosynovitis scores. ing JIA disease activity. No difference in the tenosynovial
Boxplot visualizations of total scores for a synovial thickening, b score was found between the two groups.
synovial enhancement, and c tenosynovial thickening/enhancement Separate analysis of anatomical scoring sites for
in clinically active JIA patients (left, dotted boxes) and pediatric con- synovial thickening and synovial enhancement revealed
trols (right, open boxes). ***p < 0.001, [o]: statistical outlier, “Aster-
isk” extreme statistical outlier the carpometacarpal recesses of digits 2–5, the mid-/

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Fig. 6  Grayscale map illustrating darker areas more likely to reflect

JIA disease activity than normal variance. Based on a grayscale gra-
dient, the increase in mean score within the wrist of clinically active
JIA patients, as compared to controls, have been visualized for a syn-
ovial thickening, b synovial enhancement. In this figure, darker areas
indicates the highest increase in total score, whereas lighter areas
indicates no increase in total score

inflammatory-free children, in which the distal radioulnar

was the only anatomical scoring site on which moder-
Fig. 5  For both the JIA patients (left, dotted bars) and the pediat-
ate–severe enhancement of the synovium was scored [6].
ric controls (right, open bars), the divisions of scores for a synovial Low scores for tenosynovial thickening/enhance-
thickening, b synovial enhancement, and c tenosynovial thickening/ ment were found within the wrist of clinically active JIA
enhancement. *p < 0.05, ***p < 0.001 patients. At first, this result seems contradictive to the
results published by a study on the distribution pattern
inter-carpal, the radiocarpal, and the distal radioulnar of MRI abnormalities within the joints of JIA patients,
joints to be highly affected in the wrist of clinically active which showed presence of wrist tenosynovitis in 46.5% of
JIA patients. On the contrary, the first carpometacarpal JIA patients investigated [7]. However, in that study, the
recess generated low scores for synovial thickening in JIA severity of the tenosynovial thickening/enhancement was
patients. A previous study on JIA disease activity, with- not taken into account, which might have led to an over-
out comparison to controls, revealed the distal radioulnar estimation of the contribution of tenosynovial thickening/
joint as one of the top three locations affected by synovial enhancement to overall wrist pathology in JIA patients.
thickening in the wrist of JIA patients [7]. Although the In comparison, a same approach would have generated
results of the current study are comparable to that finding, a presence of tenosynovial thickening/enhancement in
our study additionally indicates synovial thickening to be 44% of JIA patients in the current study, which is consist-
also frequently detected in the distal radioulnar joint of ent with the previous findings. Within the control group,
pediatric controls. This finding is in line with a previous tenosynovial thickening/enhancement scores were also
study on the appearance of MRI findings in the wrist of found to be low, resulting in the absence of a difference in

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tenosynovial score among clinically active JIA patients as Funding This research received no specific grant from any funding
compared to controls. agency in the public, commercial, or not-for-profit sectors.
This study encountered several limitations. First, the
establishment of a pediatric healthy control group was not Declarations
possible since it is undesirable to undergo MRI and admin-
Conflict of interest The authors declare that there is no conflict of in-
ister intravenous contrast agent to healthy children. Due to terest.
a reported prevalence of clinical arthritis in 8–12% of the
patients diagnosed with IBD, the underlying disease of in Ethics approval Approval of this study has been given by the Medical
the largest part these pediatric controls is suboptimal with Ethics Committee of the Amsterdam University Medical Centers in
Amsterdam (NL39331.018.12).
respect to the objective of the study [13, 14]. Although our
pediatric controls in this study were the best available con- Data sharing Authors are willing share data regarding our manuscript
trol population, and precautionary measures were taken to upon request.
rule out arthritis in this group, follow-up studies should aim
to include a non-inflammatory control group and acquire a Open Access This article is licensed under a Creative Commons Attri-
larger study population. Second, the controls had a signifi- bution 4.0 International License, which permits use, sharing, adapta-
cantly longer time interval from intravenous contrast admin- tion, distribution and reproduction in any medium or format, as long
as you give appropriate credit to the original author(s) and the source,
istration to image acquisition as compared to JIA patients. provide a link to the Creative Commons licence, and indicate if changes
Given the positive correlation found between post-gadolin- were made. The images or other third party material in this article are
ium time interval and synovial enhancement in the wrist of included in the article’s Creative Commons licence, unless indicated
children on contrast-enhanced MRI [15], this difference in otherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
post-contrast timing might have led to an overestimation of permitted by statutory regulation or exceeds the permitted use, you will
synovial thickening and synovial enhancement in controls. A need to obtain permission directly from the copyright holder. To view a
third limitation comprised the different MRI field strengths copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
that were applied to the two groups of children (1.5 T vs.
1.0 T, respectively), which might have influenced the assess-
ment procedure. Together, these observations indicate the
need to meticulously standardize MRI protocols with regard References
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