 SHOULDER AND ELBOW
The natural history of the rheumatoid
P. van der Zwaal,
B. G. Pijls,
B. J. W. Thomassen,
R. Lindenburg,
R. G. H. H. Nelissen,
M. A. J. van de Sande
From Leiden
University Medical
Center, Department
of Orthopaedics,
Leiden, The
Netherlands
 P. van der Zwaal, MD, PhD,
Orthopaedic Surgeon
 B. J. W. Thomassen, MSc,
Research coordinator
Department of Orthopedic
Surgery and Trauma, MC
Haaglanden, Lijnbaan32, 2501
CK, The Hague, The
Netherlands.
 B. G. Pijls, MD, PhD, Resident
Orthopaedic Surgery
 R. G. H. H. Nelissen, MD,
PhD, Orthopaedic Surgeon,
Professor
 M. A. J. van de Sande, MD,
PhD, Orthopaedic Surgeon
Department of Orthopaedics,
LUMC, Albinusdreef 2, 2300
RC, Leiden, The Netherlands.
 R. Lindenburg, MSc,
Physiotherapist
MSK Sonography Fysus
Communications, Emmapark
12, 2641 EL Pijnacker, The
Netherlands.
Correspondence should be sent
to Mr P. van der Zwaal; e-mail:
peerzwaal@hotmail.com
©2014 The British Editorial
Society of Bone & Joint
Surgery
doi:10.1302/0301-620X.96B11.
34133 $2.00
Bone Joint J
2014;96-B:1520–4
Received 16 March 2014;
Accepted after revision 1
August 2014
1520
shoulder
A PROSPECTIVE LONG-TERM FOLLOW-UP STUDY
The purpose of this study was to evaluate the natural history of rheumatoid disease of the
shoulder over an eight-year period. Our hypothesis was that progression of the disease is
associated with a decrease in function with time.
A total of 22 patients (44 shoulders; 17 women, 5 men, (mean age 63)) with rheumatoid
arthritis were followed for eight years. All shoulders were assessed using the Constant
score, anteroposterior radiographs (Larsen score, Upward-Migration-Index (UMI)) and
ultrasound (US). At final follow-up, the Short Form-36, disabilities of the arm, shoulder and
hand (DASH) Score, erythrocyte sedimentation rate and use of anti-rheumatic medication
were determined.
The mean Constant score was 72 points (50 to 88) at baseline and 69 points (25 to 100) at
final follow-up. Radiological evaluation showed progressive destruction of the peri-articular
structures with time. This progression of joint and rotator cuff destruction was significantly
associated with the Constant score. However, at baseline only the extent of rotator cuff
disease and the UMI could predict the Constant score at final follow-up.
A plain anteroposterior radiograph of the shoulder is sufficient to assess any progression of
rheumatoid disease and to predict functional outcome in the long term by using the UMI as
an indicator of rotator cuff degeneration.
Cite this article: Bone Joint J 2014;96-B:1520–4.
Patients with rheumatoid arthritis (RA) of the anteroposterior (AP) radiograph of the shoul-
shoulder joint are often diagnosed at presenta- der is positively correlated with rotator cuff
tion with at least one large tear of the rotator disease.10-12 Evaluation of the degree of peri-
cuff.1 The importance of the shoulder joint and articular damage in a rheumatoid patient with
rotator cuff to the function of the upper limb shoulder symptoms is important when decid-
mandates early detection and treatment of ing on the best treatment strategy.
imminent degeneration before the onset of an The purpose of this study was to establish
irreversible loss of function.1-3 The degree of the natural history of painful rheumatoid dis-
dysfunction of the shoulder joint is related to ease of the shoulder over an eight-year period.
the severity of the rheumatoid disease. It is Our hypothesis was that the long-term func-
believed to be caused by pain resulting from tional outcome and range of movement are not
the structural changes generated by prolifera- only associated with radiological signs of joint
tive synovitis (pannus) which leads to destruc- destruction, but also with the initial condition
tion of the joint surface, tendinitis, rotator cuff of the rotator cuff.
tears, fatty infiltration involving the muscle,
and muscle atrophy.4-6 These factors result in Patients and Methods
upward migration of the humeral head and We undertook a prospective eight-year follow-
painful subacromial impingement because of up of a previously published cohort of 26 con-
muscle imbalance and an inability of the secutive patients with rheumatoid arthritis.10
adductor muscles (teres major and latissimus There were 20 women and six men with a mean
dorsi) to co-contract to compensate.7-9 This age of 63 years (50 to 81). They were recruited
may cause further pain which, in turn, initiates at a tertiary referral centre for rheumatoid and
a vicious cycle of inactivity, pronounced fatty shoulder surgery. Inclusion was based on the
infiltration of the muscles, progression of the following criteria: a clinical diagnosis of RA
rotator cuff disease, joint destruction and fur- according to the 1987 criteria of the American
ther proximal migration of the humeral head. College of Rheumatology (formerly the Ameri-
Upward migration of the humeral head on an can Rheumatism Association);13 patient age
THE BONE & JOINT JOURNAL
 THE NATURAL HISTORY OF THE RHEUMATOID SHOULDER 1521

higher score indicates better shoulder function. To gauge

Fig. 1
Anteroposterior radiograph used
to determine the Larsen score and
to evaluate the proximal migration
of humeral head using the upward
migration index (UMI = CA/R). A,
undersurface acromion; C, centre
of the humeral head; R, radius of
the humeral head; AH, acromio-
humeral interval.
Table I. The rating of shoulder joint and rotator cuff degeneration evalu-
ated radiologically and with ultrasound
Shoulder joint destruction using the Larsen score (Larsen final follow-
up – Larsen baseline follow-up)
0 no progression
0.5 to 1 moderate progression
> 1.5 severe progression
Rotator cuff evaluation using ultrasound (ultrasound final follow-up –
Ultrasound baseline follow-up)
0 no progression
1 to 2 moderate progression
>3 severe progression
> 50 years, an age limit chosen to impose the smallest risk
from exposure to radiation (effective dose 1.6 mSv accord-
ing to European Union guidelines);14 at least one sympto-
matic shoulder and no previous trauma or surgery to the
shoulder. The study had previously received institutional
review board approval in 2004. All patients gave written
informed consent.
The degree of bone and soft-tissue involvement by rheu-
matoid disease was assessed using plain AP radiographs
and ultrasound (US) images of both shoulders. Clinical out-
come was evaluated using the Constant score (CS)15 at each
follow-up and the disabilities of the arm, shoulder and
hand (DASH) score16 only at final follow-up. The DASH
score is a patient-reported outcome measure for disability
of the upper limb which ranges from 0 (no disability) to
100 (severe disability). The Constant score (0 to 100)
assesses patient’s pain, shoulder function and strength: a
general disease activity at final follow-up, we used the short
form (SF-36) health survey17 for mental and physical state,
erythrocyte sedimentation rate (ESR < 30 mm/hr was con-
sidered active RA) and the use of anti-rheumatic medica-
tion. The mean interval between the diagnosis of RA and
the initial radiological evaluation was 13 years (1 to 40).
To assess the degree of involvement of bone and cartilage
by RA, a standard protocol AP radiograph was taken of
both shoulders of each patient in a supine position, turned
by 20° to the side of the image with the arm in external
rotation and the palm facing forward.11. The focus-to-film
distance was measured at 115 cm, and a 15° craniocaudal
tilt was used to obtain a horizontal projection of the under-
surface of the acromion, thereby giving the best approxima-
tion of a true AP projection of the glenohumeral joint
(Fig. 1). Proximal migration, an indicator for fatty degener-
ation of the rotator cuff muscles,3 was measured using the
upward migration index (UMI; UMI = CA/R), the distance
in millimetres (mm) between the centre of the humeral head
and the undersurface of the acromion (CA) divided by the
radius (R) of the humeral head (Fig. 1). A UMI of > 1.35
indicates that there is no migration; a UMI of 1.25 to 1.35
intermediate migration; and a UMI < 1.25 severe proximal
migration.3,18 All radiographs were scored by MS and PZ
at eight years follow-up for the progression of rheumatoid
disease using the Larsen score,19 which ranges from no/
slight joint space narrowing (grade 0 to 1) through destruc-
tion of the subchondral bone (grade 3), to disappearance of
original structure of the joint (grade 5) and consequently
progressive medial migration of the humeral head. A stand-
ardised ultrasound of each shoulder was carried out by an
independent, experienced musculoskeletal ultrasono-
grapher to evaluate the extent of rotator cuff pathology.
The rotator cuff was scored as follows: no tear; tendino-
pathy; small tear (< 1 cm); medium tear (1 cm to 3 cm) or
large tear (> 3 cm).20
Shoulder joint and rotator cuff degeneration were
defined as none, moderate or severe using the modified
classifications shown in Table I.
At baseline, fatty degeneration of the rotator cuff muscles,
as shown on a CT scan, was scored using the system
described by Goutallier.21 The Goutallier score is as follows:
grade 0, normal muscle quality; grade 1, some fatty streaks;
grade 2, < 50% fatty muscle atrophy; grade 3, 50% fatty
muscle atrophy and grade 4, > 50% fatty muscle atrophy.21
Statistical analysis. Due to the repeated measures design of
this study and to correct for confounding variables, a gen-
eralised mixed model was used to evaluate the radiological,
patient, and functional outcome parameters.
All parameters were checked for outliers and verified to
have a reasonably symmetrical distribution. All analyses
were performed using SPSS for Windows, version 19.0
(IBM SPSS Statistics, Chicago, Illinois) and R-statistics,
LME4 package (R-project). A p-value < 0.05 was consid-
ered statistically significant.

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1522 P. VAN DER ZWAAL, B. G. PIJLS, B. J. W. THOMASSEN, R. LINDENBURG, R. G. H. H. NELISSEN, M. A. J. VAN DE SANDE
Results
By the time of final follow-up, four patients had died from
causes unrelated to their shoulder joint or rheumatoid
arthritis and, therefore, 22 patients (44 shoulders) were
available for clinical evaluation. Of these, four did not use
any anti-rheumatic medication; seven used a single drug
(Methotrexate, Prednisone or disease-modifying antirheu-
matic drugs (DMARDs)); two used a combination of
DMARDs and non-steroidal anti-inflammatory drugs
(NSAIDs); three used a combination of methotrexate,
DMARDs and NSAIDs; and six patients used anti-tumour
necrosis factor alpha, e.g. etanercept or adalimumab, in
combination with methotrexate. Three patients (four
shoulders) had also undergone surgery on their shoulder:
one had a repair of the subscapularis tendon at six years;
one a unilateral shoulder hemiarthroplasty at one year and
one bilateral shoulder hemiarthroplasties at four and
six years. These four shoulders were excluded from the
analysis leaving 40 shoulders to review.
The Constant score decreased by a mean of three points
(53 to -37; SD 20) from 72 at baseline points (50 to 88;
SD 11) to 69 points (25 to 100; SD 19) over the eight-year
period (p = 0.39). The mean ESR at final follow-up was
17 mm/hr (2 to 45;SD 14). Full clinical and radiological
details are reported in our previous publication.10
The mean DASH score at final follow-up was 64 (29 to
95; SD 20). The mean SF-36 physical at final follow-up was
34 (13 to 37; SD 12). The mean SF-36 mental score at final
follow-up was 53 (34 to 68; SD 10).
At final follow-up, the CS was significantly associated
with the DASH score. For every one point increase in CS,
the DASH decreased by 0.7 points (95% CI 0.4 to 1.0);
p < 0.001. The CS was significantly associated with the
SF-36 physical score. For every one point increase in CS,
the SF-36 physical increased by 0.3 points (95% CI 0.1 to
0.5); p = 0.005. The CS was not significantly associated
with the SF-36 mental score; p = 0.27.
Radiological shoulder joint degeneration. Regarding the degree
of shoulder joint degeneration by Larsen score, there were
16 shoulders without progression, 18 with moderate pro-
gression and six with severe progression of joint degenera-
tion during the follow-up period. In the moderate
progression group, there was no clinically relevant or statis-
tically significant decrease in Constant score (mean
5.4 points decrease, 95% CI -5 to 15.5; p = 0.30) compared
with the no progression group.
In the severe progression group there was a clinically rele-
vant and statistically significant decrease in Constant score
(mean 27 points decrease, 95% CI 10 to 43; p < 0.001) com-
pared with the no progression group.
The mean UMI decreased significantly from 1.28
(SD 0.10) to 1.22 (SD 0.10); p < 0.001. There were five
patients with no progression (ten shoulders), seven patients
with unilateral progression (seven shoulders progression;
seven shoulders no progression) and seven patients with
bilateral progression (14 shoulders) of superior migration of
the humeral head. In one patient (two shoulders) the UMI
could not be determined due to insufficient radiographs.
Ultrasonography of rotator cuff degeneration. There were
23 shoulders without progression, 12 shoulders with mod-
erate progression and five with severe progression. In the
moderate progression group, there was no clinically rele-
vant or statistically significant decrease in Constant score
(mean 1.9 points decrease 95% CI -13 to 9.3; p = 0.74)
compared with the no progression group. In the severe pro-
gression group there was a clinically relevant and statisti-
cally significant decrease in Constant score (mean 19 points
decrease 95% CI 1.4 to 36; p = 0.02) compared with the no
progression group.
Estimation of long-term functional scores by radiological
and ultrasound evaluation. The effect of shoulder joint and
rotator cuff degeneration on Constant score at final follow-
up is shown in Table II. The presence of a large tear signif-
icantly affected the Constant score at final follow-up with a
mean decrease of 34 points (95% CI 17 to 50); p < 0.001. The
presence of tendinopathy or a small cuff tear did not signifi-
cantly affect the mean Constant score; p = 0.39 and p = 0.90.
The degree of fatty degeneration (FD) of the supraspina-
tus, infraspinatus/teres minor and subscapularis muscles at
baseline (expressed as Goutallier Score 0 to 4) also signifi-
cantly affected the mean Constant score at final follow-up.
With every unit of increased FD, the final mean Constant
score decreased by 7.4 points (95% CI 3 to 12; p < 0.01) for
the supraspinatus, 6.7 points (95% CI 2 to 12; p < 0.01) for
infraspinatus and teres minor and ten points (95% CI 4 to
17; p < 0.01) for the subscapularis. The UMI also signifi-
cantly influenced the long-term Constant score (Table II);
p = 0.02. Age (p = 0.02) and gender (p < 0.01) significantly
affected the mean Constant score at follow-up where men
presented with a higher Constant score. For every year
increase in age the Constant score decreased with 0.9
points; p = 0.02). The results presented above were there-
fore all corrected for age and gender.
Discussion
This study shows that the rheumatoid shoulder tends
towards significant radiological deterioration with time.
Furthermore, with the passage of time, rotator cuff tears
increased as did upward migration of the humeral head. As
we predicted, a worse clinical outcome (lower Constant
score) was associated with progressive joint destruction.
Deterioration of the Larsen score, the rotator cuff and the
UMI all led to a worse clinical outcome. However, the clin-
ical outcome at final follow-up was only strongly related to
the quality of the rotator cuff at baseline as evaluated by US
(tendonitis or tears), CT (Goutallier score) or radiograph
(UMI). Other baseline variables (e.g. Larsen Score) were
not related to clinical outcome. Apparently, progression of
joint destruction (Larsen Score) rather than the degree of
joint destruction at baseline may predict the functional out-
come at final follow-up. These results are in concordance
with earlier reports which looked at the association
THE BONE & JOINT JOURNAL
 THE NATURAL HISTORY OF THE RHEUMATOID SHOULDER 1523

Table II. The long-term effect of shoulder joint and rotator cuff degeneration on the mean
Constant Score (CS) (SE, standard error; UL, upper limit of 95% confidence interval; LL,
lower limit of 95% confidence interval; UMI, upward migration index)

Effect on CS* SE UL LL
Ultrasound evaluation of rotator cuff
None (reference)
Tendinopathy -4.3 4.8 -14 5
Small tear 0.8 6.1 -11 13
Large tear -34 8.5 -50 -17
Fatty degeneration Goutallier score (0 to 4)
Supraspinatus -7.4 2.4 -12 -3
Infraspinatus/teres minor -6.7 2.6 -12 -2
Subscapularis -10 3.2 -17 -4
Larsen score (1 to 5) -5.3 3.6 -12.3 2
UMI (1 to 1.5) 56 27 2.8 109
Gender 24 7.5 9.1 38
Age -0.9 0.4 -1.6 -0.2
* Corrected for age and gender

between the degree of destruction of the glenohumeral joint
and the condition of the rotator cuff at a single point in
time.10-12 The present report, as well as an earlier study,3
showed that a decrease in acromiohumeral distance as
expressed by the UMI (an indicator of rotator cuff degener-
ation) is strongly correlated with the condition of the rota-
tor cuff on US and CT; the Larsen score alone was only
moderately correlated with the US and the UMI.22
When combined, these findings indicate that progression
of disease activity in the rheumatoid shoulder can be
assessed reliably with a standard AP radiograph. This
should make it possible for physicians to predict its clinical
course and potential functional disability.
Patient-reported outcome measures (DASH score) and
health-related quality of life measures (SF-36) were signifi-
cantly associated with the Constant score. This suggests
that the progression of joint destruction and degeneration
of the rotator cuff influence patient-reported outcome
measures and the health-related quality of life in a similar
way (progression of joint destruction and degeneration of
the rotator cuff) as they influence Constant score.
The strengths of this study are its prospective design, the
long-term follow-up and the wide range of outcome meas-
ures used.
The study also has its limitations. The cohort of patients
was relatively small. Nevertheless, there was sufficient
power to identify clinically relevant effects. We recognise
that the evaluation of RA disease activity was not under-
taken using RA-specific clinical outcome measures, such as
the disease activity score23 or health assessment question-
naire.24 Future studies would benefit from correlating these
RA-specific outcome measures to specific measurements of
shoulder outcome.
Progressive destruction of the shoulder joint is associated
with poorer results from surgical intervention, whether this is
a soft-tissue procedure or joint replacement.25 Degeneration
of the rotator cuff results in a worse outcome from shoulder
replacement both in terms of function and post-operative
pain because of instability and impingement.22,25,26 In our
study, fatty degeneration of the subscapularis muscle at the
outset had the strongest influence on the long-term Constant
score, underlining its role as a prime mover.
This study shows that the progression of rotator cuff dis-
ease in the rheumatoid shoulder can be established from a
standard AP radiograph and is associated with destruction
of the joint. As UMI was strongly associated to fatty degen-
eration measured on CT we believe radiological evaluation
of the cuff using the UMI continues to be of practical use.
Unlike severe progression, moderate progression of both
radiological joint and ultrasonographic cuff deterioration
had no clinically relevant or statistically significant effect
on function. Thus moderate progression of radiological
joint and ultrasonographic cuff deterioration in the long-
term can be accepted without any serious clinical conse-
quences. Nevertheless the aim should be to minimise dete-
rioration of both joint and cuff. Signs of joint destruction
and upward migration of the humeral head using a stand-
ard AP-radiograph of the shoulder could be used to predict
clinical outcome. This can inform surgical decision-making
and thereby potentially improve the outcome of surgery.
Although none of the authors has received or will receive benefits for personal
or professional use from a commercial party related directly or indirectly to the
subject of this article, benefits have been or will be received but will be directed
solely to a research fund, foundation, educational institution, or other non-
profit organisation with which one or more of the authors are associated.
This article was primary edited by A. Ross and first proof edited by G. Scott.
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