THE PREDICTIVE VALUE OF MAGNETIC RESONANCE IMAGING FOR BONE EROSION PROGRESSION IN RHEUMATOID ARTHRITIS PATIENTS

Abstract

Objective: To determine the joint damage progression using magnetic resonance imaging (MRI), and to investigate the predictive value of early MRI for subsequent development of MRI erosions in rheumatoid arthritis (RA) patients. Methodology: We studied forty RA female patients. Their mean age was 32.7 (±8.6) years. Patients underwent clinical, laboratory and functional assessments over 12 months. Standard plain radiography and MRI of the hands and wrists were done for all patients at baseline and after 12 months. Results: all clinical and laboratory variables reflecting disease activity showed low activity after one year of treatment (p<0.05). At one year, MRI erosions were found in 62.5% of patients (25 of 40) compared with 42.5% at baseline (p<0.05). MRI findings reflecting inflammation (bone marrow edema and synovitis) regressed after one year (p<0.05). We have analyzed baseline variables for prediction of MRI erosions at one year including positive RF, plain radiological erosions, baseline MRI erosion, bone marrow edema and synovitis. Positive RF and synovitis were predictor risk factors for MRI erosive progression at one year (p<0.05). On the other hand, plain radiological erosions were not statistically significant as predictor risk factor in these patients (p>0.05). Baseline MRI erosion and bone marrow edema were strong predictors for MRI erosive progression (the odds ratio (95%CI) were 5.92 (3.06-9.03) and 12.85(3.41-21.22), respectively) (p<0.001). Conclusions: The results of this study suggest that MRI is a useful tool to investigate disease processes in RA. It can be used in clinical practice in determining the prognosis, and selecting patients who need aggressive therapy to avoid subsequent joint damage.

Full text

Egypt Rheumatol Rehab Vol. 36, No. 3, July, 2009
425
THE PREDICTIVE VALUE OF MAGNETIC RESONANCE
IMAGING FOR BONE EROSION PROGRESSION IN
RHEUMATOID ARTHRITIS PATIENTS
HALA EISSA, MOHAMMAD ABDUL- BASSETT FARAMAWY, OMAR AHMAD HASSANEIN * AND NAGWA
MAURICE WILSON ** 
Rheumatology & Rehabilitation Department, Ain Shams University Faculty Of
Medicine, Radio-Diagnosis Department, Tanta University Faculty Of Medicine* &
Ahmed Maher Teaching Hospital **
KEY WORDS: MAGNETIC RESONANCE IMAGING, RHEUMATOID ARTHRITIS, BONE EROSIONS.
ABSTRACT
Objective: To determine the joint damage progression using magnetic
resonance imaging (MRI), and to investigate the predictive value of early MRI for
subsequent development of MRI erosions in rheumatoid arthritis (RA) patients.
Methodology: We studied forty RA female patients. Their mean age was 32.7
(±8.6) years. Patients underwent clinical, laboratory and functional assessments
over 12 months. Standard plain radiography and MRI of the hands and wrists were
done for all patients at baseline and after 12 months.
Results: all clinical and laboratory variables reflecting disease activity
showed low activity after one year of treatment (p<0.05). At one year, MRI erosions
were found in 62.5% of patients (25 of 40) compared with 42.5% at baseline
(p<0.05). MRI findings reflecting inflammation (bone marrow edema and synovitis)
regressed after one year (p<0.05). We have analyzed baseline variables for
prediction of MRI erosions at one year including positive RF, plain radiological
erosions, baseline MRI erosion, bone marrow edema and synovitis. Positive RF and
synovitis were predictor risk factors for MRI erosive progression at one year
(p<0.05). On the other hand, plain radiological erosions were not statistically
significant as predictor risk factor in these patients (p>0.05). Baseline MRI erosion
and bone marrow edema were strong predictors for MRI erosive progression (the
odds ratio (95%CI) were 5.92 (3.06-9.03) and 12.85(3.41-21.22), respectively)
(p<0.001).
Conclusions: The results of this study suggest that MRI is a useful tool to
investigate disease processes in RA. It can be used in clinical practice in determining
the prognosis, and selecting patients who need aggressive therapy to avoid
subsequent joint damage.
INTRODUCTION
Rheumatoid arthritis (RA) is
characterized by inflammation of peripheral
joints that proceeds to chronic synovitis and
erosive bony change after a period of
months to years (Harris, 1990). It is a
heterogeneous disorder in terms of both
clinical presentation and outcome. In some
patients a mild, nonerosive form of RA
associated with little disability develops.
Other patients have persistent and
aggressive disease that produces severe
articular damage often requiring joint
replacement surgery after only a few years
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The Predictive Value of MRI for Bone Erosion Progression in RA Hala Eissa et al.
426
(Scott et al., 1987).
The ability to predict aggressive disease
when a patient first presents is an important
clinical goal, because this would allow
potent and potentially toxic disease-
suppressing medication to be targeted to
patients who are most in need. This
predictive ability has become even more
desirable from a medico-economic
viewpoint with the advent of anti–tumor
necrosis factor therapies, which have
powerful antierosive effects but are costly,
sometimes associated with adverse effects,
and should not be prescribed for patients in
whom the potential to develop erosions is
absent (Lipsky et al., 2000).
Many prognostic markers have been
identified for RA, including demographic,
genetic, environmental, clinical,
immunological and radiographic factors.
However, there is still a need for
development of measures that can better
distinguish between patients at risk for
radiographic progression and those with a
more favorable prognosis (Haavardsholm et
al., 2008). Magnetic resonance imaging
(MRI) is a highly sensitive method for
detecting early inflammatory and structural
abnormalities in RA and has been shown to
be better than plain radiography by a
number of authors for detection of early
rheumatoid erosions (McQueen et al., 1998
& 1999; Gilkeson et al., 1988; Foley-Nolan
et al., 1991; Ostergaard et al., 1995 and
Backhaus et al., 1999).
So MRI is increasingly recognized as
an important imaging modality to assess
disease progression in early RA and it is
likely to become an important tool in
assessing responses to disease modifying
biological agents (Kalden-Nemeth et al.,
1997), as several reports suggest that
erosions can heal in response to anti-tumour
necrosis factor á biological treatments (Rau
et al., 1999, Finck et al., 1999 and Lipsky et
al., 1999).
Aim of Work:
The aim of this prospective 1-year
follow-up study was to determine the joint
damage progression using magnetic
resonance imaging (MRI) of the hand and
wrist and to investigate the predictive value
of early MRI findings for subsequent
development of MRI erosions in rheumatoid
arthritis patients.
PATIENTS AND METHODS
Forty patients with RA of less than 2
years duration were recruited to this
prospective 1-year follow-up study. All
patients fulfilled the American College of
Rheumatology 1987 revised criteria (Arnett
et al., 1988). Their mean age (±SD) was
32.7 (±8.6) years. They were assessed
clinically at baseline for variables reflecting
disease activity including duration of
morning stiffness, 28-tender joint count (28-
TJC), 28-swollen joint count (28- SJC) and
Disease Activity Score 28 (DAS28) (Prevoo
et al., 1995) [1= low activity (score ≤ 3.2),
2= moderate disease activity (3.2< DAS28
5.1), 3 = high disease activity (score >
5.1)] (Van Gestel et al., 1998). Functional
impairment was assessed using Health
Assessment Questionnaire disability index
(HAQ DI) (Fries et al., 1980) (0= without
any difficulty, 1= with some difficulty, 2=
with much difficulty, 3= unable to do).
Laboratory assessments, including a
complete blood cell count and erythrocyte
sedimentation rate (ESR), were done at
every visit. Rheumatoid factor (RF) titer was
determined at baseline. Postero-anterior
radiographs of the hands and wrists were
obtained at baseline and at 12 months using
standardized techniques as well as MRI
scans.
MRI imaging technique:
MR imaging was performed with a 1-T
unit (Open Philips panorama high field open
[HFO] machine). The used coil was multi-
purpose medium coil. The patients were
examined in the prone position with the
hands over the head. Both hands were
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Egypt Rheumatol Rehab Vol. 36, No. 3, July, 2009
427
imaged with the extremity coil & we
selected only one hand per each patient for
the entire study to conserve the imaging
time & to prevent overtiring the patients.
The hand that appeared more significantly
involved at the outset was chosen & follow
up study of the same hand was performed.
All patients underwent imaging of the
hand and the wrist (from the ulnar styloid
process to the proximal interphalangeal
articulations). Five standard pulse sequences
were performed to the patients:
1- Coronal T1 weighted spin echo (700
/ 16 msec.) F.O.V 24cm, 256x192 matrix,
3mm section thickness.
2- Coronal T2 weighted FSE (2000 / 60
msec.) F.O.V 24cm, 256 x192 matrix, 3mm
section thickness.
3- Coronal STIR sequence (4000 / 40
/130 msec. TR / TE / TI) F.O.V 24cm,
256x192 matrix, 3mm section thickness.
4 and 5 – Coronal & axial 3D WATS
gradient sequence: (55 / 5, flip angle 45°),
F.O.V. 24cm, 256x192 matrix, 1.2mm
section thickness.
MRI scoring:
Bone erosions:
Each wrist bone (carpal bones (8),
distal radius, distal ulna (2), metacarpal
bases (5); total 15 sites) was scored
separately. The scale was 0–10, based on the
proportion of eroded bone compared with
the ‘‘assessed bone volume’’. In addition the
number of erosions at each of the 15 sites
was noted. MRI erosion score was graded on
a scale of 0–10, with each point representing
a 10% loss of bone volume.
Bone edema:
Bone edema was scored on a scale of
0–3 by the volume of edema compared with
the ‘‘assessed bone volume’’ (each wrist
bone scored separately). 0 = no edema, 1 =
1–33% of bone edematous, 2 = 34–66%, and
3 =67–100%).
Synovitis:
Synovitis in the wrist was assessed in
three regions (the distal rad³oulnar joint; the
rad³ocarpal joint; the ³ntercarpal and
carpometacarpophalangeal joints). Synovitis
was scored sem³quant³tat³vely (0–3 scale,
where 0 = normal, 1= mild, 2 = moderate,
and 3 = severe), with each point representing
one-third of the maximum volume of
enhancing tissue in the synovial
compartment.
Statistical analysis:
Study data were analyzed using the
SPSS statistical package (SPSS, version
14.0). The paired student’s t test indicates
the magnitudes of the differences of means
and SD and therefore the magnitude of the
observation. Prior to data analysis, the level
of significance was established at p<0.05.
The crosstab statistics & the Pearson chi-
square test were used to indicate the
magnitudes of the differences of percentage
of the variables. Also prediction was done
by odds ratio (OR) & confidence interval
(CI) values to define association at baseline
& after one year in patients with rheumatoid
arthritis
RESULTS
This study included forty patients with
RA. Their mean age was 32.7 (±8.6) years
whereas mean disease duration was 11.2
(±7.6) months. All patients were females,
thirty four patients were seropositive.
Table (1) presents baseline and follow-
up demographic, clinical and laboratory
characteristics of the RA patients. The study
population exhibited significant low activity
as shown by the different variables
reflecting disease activity including the
duration of morning stiffness, 28-tender
joint count, 28-swollen joint count and
disease activity score 28 [DAS28] after one
year of treatment (p<0.05). The physical
capability, expressed by the Health
Assessment Questionnaire disability index
(HAQ DI), increased at one year (p<0.001)
with a score falling from a baseline of 0.9 ±
0.3 to 0.4 ±0.2. This reflects improvement in
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The Predictive Value of MRI for Bone Erosion Progression in RA Hala Eissa et al.
428
function that paralleled a reduction in
clinical evidence of inflammation.
Meanwhile, there was a significant
improvement in laboratory markers of
inflammation (ESR) (p<0.05).
Table (1): Patients demographic, clinical and laboratory characteristics at baseline & after one year (No.=
40).
Characteristics baseline one year p value
Sex F:M
Age (years)
Disease duration (months)
Morning stiffness (minutes) (mean±SD)
28-Tender joint count (mean±SD)
28-Swollen joint count (mean±SD)
DAS28 score (mean±SD)
HAQ DI score (mean±SD)
Positive RF, no. (%)
ESR (mm/hour)
40:0
32.7 ±8.6
11.2 ± 7.6
44.8± 49.5
4.5± 3.2
2.3± 1.9
4.5±1.3
0.9± 0.3
34 (85 %)
30.3 ±21.2
-
-
-
25.6 ± 23.1*
2.8± 2.3*
1.4± 1.3*
3.6± 1.2*
0.4± 0.2**
19.8 ±16.4*
-
-
-
p<0.05 S
p<0.05 S
p <0.05 S
p <0.05 S
p <0.001 HS
-
p <0.05 S
**p<0.001= highly s³gn³f³cant (HS), *p<0.05=s³gn³f³cant (S).
Table (2): Radiological data of hands at baseline and after one year in RA patients.
Rad³olog³cal Data Basel³ne one year p value
Pla³n Rad³ography
Eros³ons, no. (%)
No eros³ons, no. (%) 8 (20%)
32 (80%) 12 (30%)
28 (70%) p>0.05 NS
-
MRI features
Eros³ons, no. (%)
No eros³ons, no. (%)
Eros³on score (mean±SD)
Bone marrow edema, no. (%)
No bone marrow edema, no. (%)
Edema score (mean±SD)
Synov³t³s, no. (%)
No synov³t³s, no. (%)
Synov³t³s score (mean±SD)
17 (42.5%)
23 (57.5%)
5.5± 2.3
22 (55%)
18 (45%)
2.4± 0.7
28 (70%)
12 (30%)
2.6± 0.8
25 (62.5%)*
15 (37.5%)
8.2± 2.6**
10 (25%)*
30 (75%)
1.3± 0.4*
10 (25%)*
30(75%)
1.3± 0.5*
p<0.05 S
-
p<0.001 HS
p<0.05 S
-
p<0.05 S
p<0.05 S
-
p<0.05 S
**p<0.001= highly s³gn³f³cant (HS), *p<0.05=s³gn³f³cant (S), p>0.05=non-s³gn³f³cant (NS)
The results of this study showed that 8
(20%) of the patients had bone erosion
detected by plain radiography while 17
[42.5%) of the patients had bone erosion
detected by MRI at baseline. There was
statistically non-significant difference
regarding frequency of erosions detected by
plain radiography in the patients at both
time points (P>0.05) (Table 2). However,
the majority of patients (25 of 40 [62.5%])
had evidence of erosions using MRI at one
year compared to at baseline (17 of 40
[42.5%)]) (p<0.05).
There was statistically highly
significant difference for MRI erosion score
between baseline and at one year (p<0.001).
MRI findings reflecting inflammation (bone
marrow edema and synovitis) regressed at
one year compared to baseline (p<0.05) as
shown in Table (2). MRI erosions scores
highly significantly progressed from
baseline to one year (p<0.001), and are
depicted in Fig. (1).
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Egypt Rheumatol Rehab Vol. 36, No. 3, July, 2009
429
Fig. (1): Box plots showing range of magnetic resonance imaging (MRI) erosion at baseline and
after one year. MRI erosion scores progressed from baseline to after one year (p<0.001).
Data were analyzed to determine how
often positive RF, plain radiological
erosions, MRI erosion, bone marrow edema
and synovitis at baseline was followed by
erosion at one year. Positive RF and
synovitis were predictor risk factors for
MRI erosive progression at one year with an
odds ratios (95%CI) of 3.72 (1.14-7.10) and
1.82 (1.12-2.70), respectively (p<0.05). On
the other hand, plain radiological erosions
were not statistically significant as predictor
risk factor in these patients. MRI erosion
and bone marrow edema were strong
predictors for MRI erosive progression with
an odds ratios (95%CI) of 5.92 (3.06-9.03)
and 12.85(3.41-21.22), respectively
(p<0.001).
Thus, those patients with bone marrow
edema at baseline were 12.85 times more
likely to develop erosions at one year than
those without bone marrow edema. Baseline
MRI bone marrow edema was strong
predictor for MRI erosive progression as
shown in Table (3).
Table 3: Baseline variables that predicted MRI erosions in the patients at one year.
MRI erosion at one year
Baseline variables Odds ratio (95%CI) P value
Positive RF
plain radiological erosions
MRI erosion
MRI bone marrow edema
Synovitis
3.72 (1.14-7.10) *
0.6 (0.2-0.9)
5.92 (3.06-9.03) **
12.85(3.41-21.22) **
1.82 (1.12-2.70) *
p<0.05 S
p >0.05 NS
p<0.001 HS
p<0.001 HS
p<0.05 S
**p<0.001= highly s³gn³f³cant, *p <0.05=s³gn³f³cant, p>0.05=non-s³gn³f³cant (NS).
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The Predictive Value of MRI for Bone Erosion Progression in RA Hala Eissa et al.
430
Fig. (2): (A&B): Baseline axial-3D-WATS gradient of the right hand revealed high signal intensity
of the distal ulna consistent with marrow edema along with thickened edematous synovium of the
distal radio-ulnar joint showing high signal intensity. (C&D) One year axial-3D-WATS revealed
multiple bony erosions of the carpal bones (capitate and scaphoid). (E) One year posteroanterior
(PA) radiograph of the same patient did not show erosions seen on MRI with normal bone
density.
DISCUSSION
The process of bone destruction in RA
is correlated with arthritis activity (Wolfe &
Sharp, 1998), although evidence is
accumulating that bone destruction can
occur independently of arthritis activity
(Mulherin et al., 1996 and Kirwan, 1997).
An important observation from our
study was the discordance between clinical
evidence of joint inflammation and MRI
findings. While clinical scores improved
during the one year study period, with
significant improvements in swollen and
tender joint counts, DAS, ESR (p<0.05) and
statistically highly significant reduction in
HAQ DI scores reflecting an improvement
in function (p<0.001), MRI erosion scores
D
C
B
A
E
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Egypt Rheumatol Rehab Vol. 36, No. 3, July, 2009
431
from our patients highly significantly
increased (p<0.001) over one year. This
striking contrast between clinical
improvement and imaging deterioration goes
in harmony with the results of McQueen et
al. (1999), Brown et al. (2008). McQueen et
al. (1999) found interesting disparity
between clinical improvement of joint
inflammation and MRI findings. While
clinical scores improved during the study
period, with significant reductions in
swollen and tender joint counts, HAQ DI
scores, CRP and ESR, MRI synovitis scores
did not improve during the same period.
They explained this by the fact that MRI
may detect subclinical synovitis that could
persist despite apparent clinical
improvement and the pathological processes
underlying joint inflammation may differ
from those resulting in erosion and articular
damage. They added that biological agents
may allow these processes to be targeted
separately and MRI scans could play a
useful part in evaluating their influence on
disease progression in early RA.
Fig. (3): (A): One year posteroanterior (PA) radiograph of another patient, no radiological signs of
rheumatoid activity could be detected. (B): One year coronal STIR sequence of both hands,
showed multiple tiny bony erosions of the carpal bones (foci of high signal intensity). (C&D) One
year coronal T1 sequence of both hands, revealed multiple foci of low T1 signal intensity within
the carpal bones consistent with tiny erosions.
Brown et al. (2008), reported that
traditional measures used to assess disease
activity in RA, largely rely on subjective
clinical symptoms, joint examination
findings, and laboratory measures of acute-
phase reactants, which are not sufficiently
sensitive to exclude ongoing inflammation
in patients with low levels of disease activity
and may also lack predictive validity since
they are unable to accurately predict
subsequent structural deterioration as early
as 1 year later. Their study data support the
hypothesis that subclinical inflammation,
which is undetectable by traditional
A
B
D
C
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The Predictive Value of MRI for Bone Erosion Progression in RA Hala Eissa et al.
432
measurement techniques, is the
pathophysiologic mechanism for continued
structural progression in RA despite
apparent clinical improvement.
Early initiation and optimal adjustment
of effective treatments requires early
diagnosis and sensitive monitoring of the
disease process. So we have to focus on
reliable prognostic markers to allow
stratification of patients to individually
tailored treatments, with particular reference
to biological agents (Lindegaard et al.,
2006).
We have shown 42.5% of our patients
to have MRI erosions at baseline and this
increased to 62.5% at one year. This was
different than radiological erosions that
increased from 20% to 30% over the same
period. This is in agreement with the results
of McQueen et al. (1999). Their study
showed that at one year, MRI erosions were
found in 74% of patients (31 of 42)
compared with 45% at baseline. Twelve
patients (28.6%) had radiographic erosions
at one year. They stated that it is important
to know whether MRI erosions are early
transient lesions or whether they are
persistent and associated with progressive
joint damage. Their and our results suggest
that the latter is generally true. They added
that the relation between MRI and
radiological erosions is also important to
define and radiological erosions may be
underestimated because of the difficulty in
visualizing radiological erosions in the
carpus because of its three dimensional
structure and because that in some patients,
radiological erosions may take longer to
develop.
MRI signs of inflammation, both
synovitis and bone marrow edema, were
markedly reduced during our study, and
coincided with reduction in clinical and
biochemical markers of disease activity. At
baseline, the synovitis score was 2.6±0.8
and reduced to 1.3±0.5 after one year.
Similarly, the edema score was 2.4±0.7 then
reduced to 1.3±0.4 at 1 year. This is in
accordance with Ostergaard & co-workers
(1999) and Lindegaard et al. (2006).
Our study showed that positive RF was
predictor risk factor for MRI erosive
progression at one year with an odds ratios
of 3.72 (1.14-7.10) (p<0.05). This is in
agreement with McQueen et al. (2001), who
reported that a positive rheumatoid factor
was likely to have influenced erosion
development (P=0.08) in their study, and
this might have reached significance in a
larger studied group.
We have analyzed baseline MRI scans
to look for early changes that may precede
joint erosion at one year. Baseline MRI
erosion and bone marrow edema were strong
predictors of MRI erosion at one year and
seem to be early indicators of potentially
aggressive disease. Baseline MRI bone
marrow edema was an important predictor
for MRI erosive progression with an Odd
ratio of 12.85 (3.41-21.22). This is in
agreement with the results of McQueen et al
(1999, 2001 and 2003), Lindegaard and
associates (2006) and Haavardsholm and
co-workers (2008). McQueen et al (1999,
2001 and 2003) studies data showed that
both MRI bone erosion and bone marrow
edema in patients with early rheumatoid
arthritis have been shown to predict future
radiographic lesions in cohorts followed for
up to 6 years. Haavardsholm et al. (2008)
identified bone marrow edema as an
independent predictor of progression of joint
damage evaluated by both MRI and
conventional radiography.
Bone marrow edema has long been
recognized as being important in RA
pathology and has been assumed to
represent inflammatory activity within the
bone (McQueen & Ostendorf, 2006). The
basic mechanism underlying the association
between MRI bone marrow edema and
erosions has been discussed in studies
published by Jimenez-Boj et al. (2007) and
McQueen et al. (2007). They suggested that
MRI bone erosions and MRI bone marrow
edema are due to formation of inflammatory
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Egypt Rheumatol Rehab Vol. 36, No. 3, July, 2009
433
infiltrates in the bone marrow of patients
with RA, and thus represent an additional
target structure for anti-inflammatory
treatment.
Our study showed a significant
association between baseline synovitis and
subsequent development of MRI erosions at
one year with an Odd ratio of 1.82 (1.12-
2.70). This is in agreement with the results
of the study done by Ostergaard et al.
(1999) and Conaghan et al. (2003). They
stated that MRI scores of synovitis were
strongly correlated with the subsequent
development of MRI erosions, supporting
the close relationship between the extent of
MRI synovitis and the risk of developing
structural joint damage observed in studies
using high-field MRI. Similarly, this came
in agreement with Lindegaard & associates
(2006) who stated that with MRI synovitis at
baseline (grades 1–3), the relative risk of
having MRI erosions at the 1-year follow-up
was 7.3, compared without MRI synovitis
(grade 0).
In summary, we found that structural
progression occurs in RA patients despite
the presence of clinical improvement and
MRI of the hand and wrist in RA may help
to predict erosive outcome at one year.
Conclusions:
The present study supports the use of
sensitive imaging techniques for the
accurate evaluation of disease status and the
prediction of outcome in patients with RA,
even when the findings of standard clinical
measures of inflammatory activity have
returned to normal. Furthermore, an
objective imaging assessment improves the
sensitivity of inflammation detection,
enabling more-informed treatment decisions
and help clinicians to determine which
patients need early and aggressive treatment
to avoid subsequent joint damage.
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The Predictive Value of MRI for Bone Erosion Progression in RA Hala Eissa et al.
436
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