Rheumatology 2011;50:410–416
doi:10.1093/rheumatology/keq335
Advance Access publication 8 November 2010
RHEUMATOLOGY
Original article
Development of a computed tomography method
of scoring bone erosion in patients with gout:
validation and clinical implications
Nicola Dalbeth1,2, Anthony Doyle3,4, Lucinda Boyer4, Keith Rome5,
David Survepalli5, Alexandra Sanders5, Timothy Sheehan4, Maria Lobo2,
Greg Gamble1 and Fiona M. McQueen2,6
Abstract
Objectives. To develop a method of scoring bone erosion in the feet of patients with gout using CT as
an outcome measure for chronic gout studies, consistent with the components of the OMERACT filter.
Methods. Clinical assessment, plain radiographs and CT scans of both feet were obtained from
25 patients with chronic gout. CT scans were scored for bone erosion using a semi-quantitative
method based on the Rheumatoid Arthritis MRI Scoring System (RAMRIS). CT bone erosion was assessed
at 22 bones in each foot (total 1100 bones) by two independent radiologists. A number of different models
were assessed to determine the optimal CT scoring system for bone erosion, incorporating the frequency
of involvement and inter-reader reliability for individual bones.
CLINICAL
SCIENCE
Results. An optimal model was identified with low number of bones required for scoring (seven bones/
foot), inclusion of bones over the entire foot, high reliability and ability to capture a high proportion of
disease. This model included the following bones in each foot: first metatarsal (MT) head, second to fourth
MT base, cuboid, middle cuneiform and distal tibia (range 0–140). Scores from this model correlated with
plain radiographic damage scores (r = 0.86, P < 0.0001) and disease duration (r = 0.42, P < 0.05). Scores
were higher in those with clinically apparent tophaceous disease than in those without tophi (P < 0.0001).
Conclusions. We have developed a preliminary method of assessing bone erosion in gout using conventional CT. Further testing of this method is now required, ideally in prospective studies to allow analysis of
the sensitivity to change of the measure.
Key words: Gout, Erosion, Computed tomography, Tophus.
Introduction
Bone erosion is a frequent manifestation of chronic gout.
These lesions contribute to deformity, limitation of joint
movement and musculoskeletal disability in patients
with gout [1, 2]. Given the clinical importance of this
1
Department of Medicine, University of Auckland, 2Department of
Rheumatology, Auckland District Health Board, 3Department of
Anatomy with Radiology, University of Auckland, 4Department of
Radiology, Auckland District Health Board, 5Department of Podiatry,
AUT University and 6Department of Molecular Medicine and
Pathology, University of Auckland, Auckland, New Zealand.
Submitted 25 June 2010; revised version accepted 2 September 2010.
Correspondence to: Nicola Dalbeth, Bone and Joint Research Group,
Department of Medicine, Faculty of Medical and Health Sciences,
University of Auckland, 85 Park Rd, Grafton, Auckland, New Zealand.
E-mail: [email protected]
pathological change, reliable assessment of the extent
of bone erosion is important. In particular, the recent
development of highly effective urate-lowering therapies
and other agents that may prevent or even reduce bone
erosion highlights the importance of developing a robust
outcome measure for reporting bone erosion in clinical
trials of chronic gout.
The optimal method of quantifying structural articular
damage in chronic gout has not been determined to
date. We have previously validated a plain radiographic
damage score for use in chronic gout, modified from the
Sharp–van der Heijde method for RA [3]. However, plain
radiography may not be optimal as the sole assessment
tool of structural change in chronic gout as it has lower
sensitivity and specificity for bone erosion compared with
other advanced imaging methods [1, 4]. Furthermore, the
! The Author 2010. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: [email protected]
CT erosion scoring in gout
validated radiographic damage score, which is weighted
in favour of the hands and includes only the forefoot, may
not comprehensively capture affected sites in gout, a disease with a marked predilection for the foot.
Conventional CT has high sensitivity and specificity for
detection of tophi, and has been used to reliably estimate
tophus size [5, 6]. This method also has superior ability to
detect bone erosion in erosive arthropathies such as RA,
compared with both plain radiography and MRI [7, 8]. In a
study examining the mechanisms of bone erosion in gout,
we have recently demonstrated that CT can reliably
assess erosion size in the hands of patients with chronic
gout, using a manual quantitative method of recording
the longest erosion diameter in the axial plane [1]. This
quantitative method was reliable, but was considered
too labour intensive for comprehensive assessment of a
large number of scans, as would be required in a clinical
trial with bone erosion as an outcome measure.
The aim of this study was to develop a preliminary CT
method of scoring bone erosion in the foot and ankle for
use in clinical trials of chronic gout, consistent with the
components of the OMERACT filter [9]. We considered
that an ideal CT bone erosion scoring system should
have the following properties for use in gout studies:
fewest number of bones within the model (feasibility);
high inter-observer reliability (discrimination); inclusion of
sites most frequently affected by gout (validity); association with other measures of chronic gout severity such
as disease duration and presence of tophi (validity); and
association with other radiographic features of chronic
gout severity (validity).
Patients and methods
Patients
Twenty-five adult patients with gout were recruited from
rheumatology outpatient clinics in Auckland, New
Zealand. The Northern Y Regional ethics committee
approved the study and patients provided written informed consent according to the Declaration of Helsinki.
All patients had a history of acute gout according to the
ACR diagnostic criteria [10], and were excluded if they
were experiencing an acute gout flare at the time of assessment, had lower limb amputation or diabetes mellitus.
Information regarding age, gender, ethnicity, disease duration, presence of subcutaneous tophi at any site and in
the feet and other clinical characteristics of gout were recorded. Blood samples were obtained for measurement
of serum urate and CRP on the day of assessment.
CT scans
CT scans of the feet and ankles were performed on a
Philips Brilliance 16-slice scanner (Philips Medical
Systems, Best, The Netherlands). The patients were positioned supine with the knees bent at 90 and the feet
dorsiflexed 45 . Both feet were scanned together with
the CT gantry vertical. The range covered was from
5 cm above the ankle joint to the ends of the toes. All
scans were performed with the same image protocol:
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acquisition at 16 0.75 mm, reconstructed on a bone algorithm, 768 matrix, to 0.8 mm slices with a 0.4 mm increment (kVp 140, 120 mAs/slice). Additional reconstructions
were done on a soft tissue algorithm, 512 matrix, also to a
0.8 mm slice with a 0.4 mm increment. The images were
viewed as 0.8 mm slices on a Philips CT workstation and
reconstructed to 3 mm slices for viewing on a picture
archiving communication system (PACS).
CT scans were analysed for bone erosion by two independent musculoskeletal radiologists (A.D. and L.B.) who
were blinded to the clinical details, plain radiographic
damage scores and each other’s CT erosion scores. The
radiologists used the overlapping thin slices to interactively
generate multiplanar reformations on standard PACS
workstations (Impax version 4; Agfa-Gevaert, Mortsel,
Belgium; and Osirix version 3.6; Osirix Foundation,
Geneva, Switzerland). Bone erosion was assessed using
reformatted images in the anatomical, axial, sagittal and
coronal planes. Erosions on CT were defined as focal
areas of loss of cortex with sharply defined margins,
seen in two planes, with cortical break seen in at least
one plane. Bone erosion was scored using a semiquantitative method based on the rheumatoid arthritis
MRI scoring system (RAMRIS) [11]; each bone was
scored separately on a scale from 0 to 10, based on the
proportion of eroded bone compared with the ‘assessed
bone volume’, judged on all available images—0: no erosion; 1: 1–10% of bone eroded; 2: 11–20%, etc. For long
bones and large tarsal bones, the ‘assessed bone volume’
was from the articular surface (or its best estimated position if absent) to a depth of 1 cm. Bone erosion was assessed at 22 bones in each foot (44 bones/patient) and in a
total of 1100 bones. These sites were selected to include
all bones in the foot and ankle except for the great toe
distal phalanx and the lesser toe phalanges. The following
bones were scored: distal and proximal portions of the first
proximal phalanx, first to fifth metatarsal (MT) heads, first
to fifth MT bases, lateral, middle and medial cuneiforms,
navicular, cuboid, anterior process of calcaneus, proximal
calcaneus, distal talus, proximal talus and distal tibia.
Plain radiographs
Plain radiographs of both feet (posteroanterior views)
were obtained on the same day as the clinical assessments and CT scans. The plain radiographs were assessed by a rheumatologist (N.D.) with experience in
scoring of gout radiographs who was blinded to the clinical details and CT scores. The films were scored using
the gout radiographic damage method that we have recently validated using a separate set of radiographs, with
excellent inter- and intra-observer reliability [3]. This
method includes scoring each joint for erosion (0–10)
and joint space narrowing (0–4) at the first to fifth MTP
joints (MTPJs) and first toe IP joint (IPJ), with a maximum
total score of 168 in the feet.
Statistical analysis
Data were analysed using Prism v5 (GraphPad; San
Diego, CA, USA) and SPSS v15 (SPSS, Chicago, IL,
411
Nicola Dalbeth et al.
USA). Medians with ranges and percentages were used to
describe the clinical characteristics. Individual bones were
analysed to determine the frequency of erosion, interobserver agreement and Cohen’s k-value. Reliability of
the erosion scores of individual bones was also assessed
using inter-observer intra-class correlation coefficients
(ICCs). Mean erosion scores for individual bones were
used for the model analysis. A variety of models were
assessed based on analysis of the individual bone data
including combinations of scores from those sites where
525% of bones were affected by erosion and/or exclusion of those individual bones where inter-observer ICC
was low (<0.70 or <0.80). These models were compared
with the combined scores for all bones and for just the first
MT heads. The inter-observer reliability of these models
was assessed by ICC and Bland–Altman limits of agreement analysis. Correlations between clinical, plain radiographic and CT data were analysed by Spearman
correlations. Comparison between groups was done
using the Mann–Whitney U-test in the case of two
groups and the Kruskal–Wallis test with Dunn’s post test
in the case of more than two groups. All tests were two
tailed and P < 0.05 was considered to be statistically
significant.
Results
Clinical characteristics
Of the 25 patients, 19 (75%) were male, 17 (68%) were
non-Polynesian and 8 (32%) were of Maori or Pacific ancestry. The median (range) age was 60 (37–83) years, disease duration was 21 (1–50) years and flare frequency was
2 (0–15)/year. Thirteen (52%) patients had clinical evidence of tophaceous disease at any site, 11 (44%) had
microscopically proven disease and 22 (88%) were on
regular urate-lowering therapy (21 on allopurinol, 1 on probenecid). The median (range) number of s.c. tophi apparent in the feet on physical examination was 0 (0–7). The
median (range) serum urate was 0.35 (0.14–0.61) mmol/l
and CRP was 2.7 (<1–29) mg/l. The median (range) radiographic damage score for the feet was 17 (0–70).
CT assessment of individual bone erosion
Erosion was reported to be present by both observers in
384/1100 (34.9%) bones, to be present by one observer in
171/1100 (15.5%) bones and to be absent by both observers in 545/1100 (49.5%) bones. For those erosions that
were identified by both observers, the median (range)
erosion score was 2 (1–10). Examples of the range of
CT bone erosions are shown in Fig. 1. CT bone erosion
was reported by both observers in 188/600 (31.3%) bones
of the forefoot; affecting 70/150 (46.6%) bones of the
great toes, 18/200 (9.0%) bones of the lesser toes and
100/250 (40%) of the MT bases (Table 1). Erosion was
also apparent in 129/250 (51.6%) bones of the mid-foot
and 67/250 (26.8%) bones of the rear foot and ankle.
Overall, there was 84% agreement between observers
regarding the presence of individual bone erosions on CT
scanning [Cohen’s k (95% CI) 0.68 (0.64, 0.73)]. Those
erosions with agreement between observers were larger
than those without agreement; median (range) erosion
score was 2 (1–10) vs 0.5 (0.5–3), respectively,
P < 0.0001. For all individual bones, the inter-observer
ICC (95% CI) for erosion score was 0.80 (0.78, 0.82).
When there was agreement on the presence of erosion,
the inter-observer ICC (95% CI) for erosion score was
0.86 (0.84, 0.87).
Models of CT bone erosion scoring
In order to develop a feasible, reliable and valid CT bone
erosion scoring method, a variety of models were assessed based on analysis of the individual bone data
(Table 1). This included analysis of combinations of
scores from those sites where 525% of bones were
affected by erosion and/or exclusion of those individual
bones where inter-observer ICC was low (<0.70 or
<0.80; Table 2). Based on this exercise, Model 5 was
considered the optimal model due to the low number of
bones required for scoring (seven bones/foot), high reliability and ability to capture a high proportion of disease
(Table 2). Model 5 consisted of individual sites where
525% of bones were affected by erosion and excluded
all bones with ICC <0.8. Model 6 (the sum of the first MT
head erosion scores) required scoring of only two bones
per patient and captured the highest proportion of disease. However, Model 6 was less reliable with lower
ICCs and higher limits of agreement (proportional to the
median erosion score) compared with the other models
(Table 2). Bland–Altman plots are shown for each model
in supplementary figure 1 (available as supplementary
data at Rheumatology Online).
Model 5 consisted of the sum of erosion scores from
the following bones in each foot: first MT head, second
MT base, third MT base, fourth MT base, cuboid, middle
cuneiform and distal tibia (Fig. 2). For all of the bones
included in this model, there was agreement between
FIG. 1 Examples of CT bone erosion at the first MT head. Representative images are shown with the corresponding
individual bone erosion score.
412
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80
66
98
90
92
96
92
82
88
88
86
74
86
90
90
76
86
78
72
76
90
86
Site
Distal portion of the first proximal phalanx
Proximal portion of the first proximal phalanx
First MT head
Second MT head
Third MT head
Fourth MT head
Fifth MT head
First MT base
Second MT base
Third MT base
Fourth MT base
Fifth MT base
Lateral cuneiform
Middle cuneiform
Medial cuneiform
Navicular
Cuboid
Anterior process of calcaneus
Proximal calcaneus
Distal talus
Proximal talus
Distal tibia
Agreed by both observers.
a
Inter-reader agreement
regarding presence
of erosion, %
TABLE 1 Individual sites of CT bone erosion
0.59
0.34
0.94
0.64
0.00
0.73
0.77
0.63
0.75
0.76
0.72
0.48
0.71
0.80
0.79
0.52
0.72
0.52
0.34
0.27
0.80
0.72
(0.39,
(0.10,
(0.82,
(0.36,
(0.00,
(0.38,
(0.56,
(0.42,
(0.56,
(0.58,
(0.52,
(0.24,
(0.51,
(0.63,
(0.61,
(0.31,
(0.52,
(0.27,
(0.08,
(0.00,
(0.63,
(0.54,
0.80)
0.58)
1.00)
0.93)
0.01)
1.00)
0.98)
0.83)
0.94)
0.94)
0.91)
0.72)
0.90)
0.97)
0.96)
0.74)
0.91)
0.77)
0.61)
0.57)
0.97)
0.90)
Inter-reader
Cohen’s i
(95% CI) regarding
presence of erosion
14
17
39
6
0
3
9
14
26
22
22
16
27
26
29
23
24
12
8
6
23
18
(28)
(34)
(78)
(12)
(0)
(6)
(18)
(28)
(52)
(44)
(44)
(32)
(54)
(52)
(58)
(46)
(48)
(24)
(16)
(12)
(46)
(36)
Number (%) of
bones with CT
erosion presenta
0.74
0.51
0.91
0.88
0.00
0.72
0.78
0.72
0.81
0.92
0.87
0.64
0.66
0.91
0.78
0.73
0.82
0.61
0.21
0.44
0.76
0.80
Inter-reader
ICC CT erosion
score
0 (0–7.5)
1 (0–9)
2.75 (0–10)
0 (0–5)
0 (0–1.5)
0 (0–2.5)
0 (0–3)
0 (0–3.5)
1 (0–6)
0.5 (0–7)
0.5 (0–6)
0.5 (0–5)
1 (0–3.5)
1 (0–5.5)
1 (0–4)
0.75 (0–5)
0.5 (0–4)
0 (0–2.5)
0 (0–2)
0 (0–3)
0.5 (0–3.5)
0.25 (0–3.5)
Median (range)
CT erosion score
CT erosion scoring in gout
413
Nicola Dalbeth et al.
TABLE 2 Characteristics of CT bone erosion models: scores and reliability analysis
All bones
Model 1
Model 2
Model 3
Model 4
Model 5
Model 6
Number of
bones
scored/foot
Maximum
possible CT
erosion score
Median CT
erosion score
(range)
Median score/number
of bones assessed
22
15
15
12
8
7
1
440
300
300
240
160
140
20
29 (5–106.5)
28 (4.5–87.5)
23.5 (4.5–73.5)
23.5 (4.5–67.5)
14 (3–52.5)
13.5 (3–52.5)
5.5 (0–15)
0.66
0.93
0.78
0.98
0.88
0.96
2.75
Inter-reader ICC
(95% CI)
CT erosion score
0.92
0.93
0.94
0.94
0.95
0.96
0.87
(0.82,
(0.85,
(0.86,
(0.87,
(0.90,
(0.90,
(0.73,
0.96)
0.97)
0.97)
0.97)
0.98)
0.98)
0.94)
Inter-reader
bias (S.D.)
1.7
0.5
0.2
0.4
2.1
2.1
1.4
(12.9)
(10.1)
(8.1)
(7.3)
(4.7)
(4.4)
(2.4)
Model 1: sum of erosion scores from sites with 525% of bones involved; Model 2: sum of erosion scores from sites with ICC
50.7; Model 3: sum of erosion scores from sites with ICC 50.7 and 525% of bones involved; Model 4: sum of erosion
scores from sites with ICC 50.8; Model 5: sum of erosion scores from sites with ICC 50.8 and 525% of bones involved and
Model 6: sum of erosion scores from first MT heads only.
FIG. 2 Sites for scoring in Model 5. Three-dimensional CT
dorsoplantar images of the foot and ankle bones with sites
for scoring highlighted.
compared with each site]. All other sites contributed
equally to the overall score, ranging from 6.7 to 12.2%.
Properties of the CT erosion models
Scores from all CT models correlated highly with the gout
plain radiographic damage score, another measure of
structural joint damage in gout (Table 3). The models
also correlated strongly with the number of tophi affecting
the feet on physical examination and weakly with disease
duration (Table 3). There was no correlation between
serum urate at the time of the study visit and CT erosion
scores. Of note, correlations with Model 5 were similar or
higher compared with those observed with the other
models tested (Table 3).
Scores for Model 5 were higher in those with any clinically apparent tophaceous disease than those without
tophi; median (range) 27 (9.5–52.5) vs 6.5 (3–15), respectively, P < 0.0001. No relationship was found between the
models of bone erosion and flare frequency, microscopically proven disease or CRP (data not shown).
Discussion
readers regarding the presence of
Cohen’s k values in >0.70 (Table
scores contributed most to the
model [median (range) 34.7%
414
erosion in >85% and
1). The first MT head
overall score in this
(0–100%), P < 0.05
Feasible, reliable and valid outcome measures to assess
structural damage are considered essential in the study of
erosive arthropathies. Here, we have developed a CT
method for quantifying bone erosion, a key pathology in
chronic gout. The proposed method appears to be feasible, has high inter-observer reliability, captures bones
most frequently affected by gout, correlates well with
other measures of gout severity and distinguishes between mild and severe chronic gout.
An important aim of this analysis was to identify patterns of bone involvement in gout in order to remove
less-affected sites from the scoring system, thus improving the efficiency and feasibility of the scoring system,
while maintaining its validity. The pattern of bone erosion
is similar to the pattern of involvement classically affected
by acute gout [10], providing further construct validity to
the scoring system. The relative sparing of certain bones
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CT erosion scoring in gout
TABLE 3 Spearman correlation (r) between CT erosion
scoring models and other measures of disease severity
All bones
Model 1
Model 2
Model 3
Model 4
Model 5
Model 6
Disease
duration
Number of s.c.
tophi affecting
the feet
0.41*
0.41*
0.44*
0.41*
0.43*
0.42*
0.36
0.78***
0.77***
0.79***
0.79***
0.82***
0.82***
0.76***
Plain
radiographic Serum
damage score urate
0.89***
0.86***
0.86***
0.84***
0.87***
0.86***
0.86***
0.05
0.08
0.07
0.05
0.15
0.14
0.18
Model 1: sum of erosion scores from sites with 525% of
bones involved; Model 2: sum of erosion scores from sites
with ICC 50.7; Model 3: sum of erosion scores from sites
with ICC 50.7 and 525% of bones involved; Model 4: sum
of erosion scores from sites with ICC 50.8; Model 5: sum of
erosion scores from sites with ICC 50.8 and 525% of
bones involved and Model 6: sum of erosion scores from
first MT heads only. *P < 0.05; ***P < 0.0001.
within the foot, such as the lesser toe MT heads, raises
interesting questions about why MSU crystals preferentially deposit at certain sites and not at others. It is conceivable that those sites frequently affected by bone
erosion in gout, such as the first MT head, mid-foot and
tibiotalar joints, are at particular risk due to greater biomechanical loading during the gait cycle. Such loading
may lead to debris within the joint that can provide a nucleus for crystal formation [12], or trigger release of microcrystals from preformed deposits within the joint.
Alternatively, this loading may alter the cellular composition or response to existing MSU crystals within the joint,
in turn promoting a local inflammatory or catabolic tissue
response [13]. The patterns of involvement also have
some clinical relevance: emphasizing the importance of
assessing frequently affected sites in the gouty foot and
suggesting a potential role of specific foot orthoses to
improve pain and function as adjunctive treatment in
chronic gout.
The observed pattern of bone involvement further
argues for the role of a CT bone erosion scoring system
in addition to the plain radiographic damage score as an
outcome measure in studies of articular damage in chronic gout. The validated gout radiographic damage-scoring
method includes both the hands and the feet, and only the
MTPJs and first toe IPJ in the feet [3]. Although the first
MT head score was the greatest single contributor to the
CT bone erosion score, 65% of the overall CT score was
derived from more proximal sites, which are poorly assessed by plain radiography. Thus, CT allows assessment
of pathology not readily captured by plain radiography.
This study has shown good overall inter-reader reliability using a semi-quantitative method of erosion scoring.
This reliability is equivalent to our previous analysis using
a quantitative measurement of erosion size by recording
the longest diameter in the axial plane [1]. The semiquantitative scoring system used in the current study
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has been validated for use in the assessment of bone
erosion in RA [7, 11] and has the particular advantages
of assessment of erosion size in three dimensions and
ease of measurement. Of note, use of this semiquantitative method for scoring of CT erosion in RA has
been shown to correlate well with more complex and
labour-intensive quantitative methods of manually measuring erosion by CT [8].
As with our previous analyses of the mechanisms of
bone erosion in gout, we have confirmed the close relationship between tophi and bone erosion in the feet [1, 3].
The current results have particular relevance for the
design of clinical trials in chronic gout where bone erosion
is an outcome measure. The higher erosion scores in
those patients with clinically apparent tophaceous disease argue for specific inclusion of patients with tophi at
baseline, as these patients are more likely to have erosive
disease. Such inclusion criteria are likely to allow greater
ability to detect change and avoid floor effects of the
measure. Additional work is required before this scoring
system can be widely introduced for the purposes of outcome measurement in clinical trials of gout. Further validation is now required using a larger data set, with analysis
of the sensitivity to change of this method. Of particular
interest will be the comparison between CT and plain radiography in longitudinal studies, noting the additional expense, time requirements and radiation exposure of CT.
Although the inter-observer limits of agreement (proportional to the median score) were lowest using Model 5,
and were also lower than those previously reported for
the plain radiographic damage score [3], measurement
variation for the proposed CT model was observed; this
variation may limit the ability of this method to detect significant and clinically relevant changes over time.
In summary, we have developed a preliminary method
of assessing bone erosion in gout using conventional CT.
This method meets many components of the OMERACT
filter for use as an outcome measure in studies of chronic
gout [14]. Further testing of this method is now required,
ideally in prospective studies to allow analysis of the sensitivity to change of this measure.
Rheumatology key messages
A CT bone erosion score has been developed for
clinical trials in gout.
. The gout CT bone erosion scoring method fulfils
many aspects of the OMERACT filter.
. Bone erosion in gout most frequently affects the
first MT head and mid-foot bones.
.
Acknowledgements
Funding: This work was supported by AUT University and
the JD Findlay Trust.
Disclosure statement: The authors have declared no
conflicts of interest.
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