ARTICLE
Auteur(s) :, Paolo Gisondi1,2, Giampiero
Girolomoni2, Francesca Sampogna1, Stefano
Tabolli1, Damiano
Abeni1,*
1Istituto Dermopatico dell’Immacolata, IRCCS, Via
Monti di Creta 104, 00167 Roma, Italy.
2Department of Biomedical and Surgical Sciences, Section
of Dermatology, University of Verona, 37126 Verona, Italy
accepté le 11 Mars 2005
Psoriatic arthritis (PsA) is a chronic inflammatory arthropathy
closely associated with psoriasis [1]. The European
Spondyloarthropathy Study Group (ESSG) has included PsA in the
group of seronegative spondyloarthropathies together with
ankylosing spondylitis, arthritis of inflammatory bowel disease and
Reiter disease, and has also introduced currently used
classification criteria [2]. PsA may be a severe and disabling
disease, in which early diagnosis is crucial to introduce a
disease-modifying therapy. Different data have been reported on the
prevalence of PsA in patients with psoriasis, ranging from 6.2% to
34.4% in different studies [3-10]. In the USA, a recent National
Psoriasis Foundation survey reported that approximately 23% of
people who have psoriasis have PsA [11]. However, the general
consensus is that prevalence ranges from 7 to 10% [12-15]. It is
conceivable that discrepancies in prevalence estimates could depend
on applying different diagnostic criteria, different sampling of
patients, as well as real variations in the prevalence and
expression of PsA in different populations. In most cases, PsA
develops after skin disease making the dermatologist the physician
who should recognise and treat early-phase PsA. However, patients
with plaque psoriasis may complain of musculoskeletal symptoms not
necessarily related to PsA, similarly to people without psoriasis
[16]. Therefore, there is a need to distinguish patients with PsA
from those with psoriasis and joint complaints in order to
accurately diagnose PsA. The objective of our study was to estimate
the prevalence of PsA, and joint signs and symptoms in a large
population of Italian patients with skin psoriasis.
Materials and methods
Study population
This study was part of a wide clinical and epidemiological study on
psoriasis, the Italian Multipurpose Psoriasis Research on Vital
Experiences (IMPROVE) study [17]. Patients were recruited between
February 21st 2000 and February 19th 2002 at
the inpatient wards of our Institute. During the study period a
wide range of psoriasis patients were hospitalised. The indications
for the hospitalisation of the patients were mainly the severity of
psoriasis and PsA requiring close assistance. However,
hospitalisation was also provided to patients with moderate
clinical disease severity in order to supply them with treatment
and diagnostic procedures that may not be available in their
regions of residence (e.g., phototherapy, magnetic resonance
imaging). The study was approved by the Institutional Review Board.
Patients admitted with a diagnosis of psoriasis were contacted by
our dermatologists, who verified the diagnosis and the inclusion
criteria (i.e., 18 years of age or more, absence of any severe
mental illness, at least 5 years of education, ability to read
Italian, first hospitalisation for psoriasis since the date of the
beginning of the study), and explained the purposes and methods of
the study to the patients. All eligible patients who gave their
written informed consent were recruited in the study. In this
analysis we considered patients with PsA and patients with chronic
plaque psoriasis in order to obtain meaningful comparisons between
patients with PsA and a homogeneous and sufficiently large group of
psoriasis patients.
Assessment of PsA and joint complaints
PsA belongs to a group of inflammatory arthritic conditions called
the spondyloarthropathies, which also include reactive arthritis,
ankylosing spondylitis and enteropathic arthropathy. This group
shares some characteristics that have been defined in the ESSG
criteria [2]. According to these criteria we classified a psoriatic
patient as affected by PsA when he showed asymmetric or
predominantly lower extremity synovitis or inflammatory spinal pain
plus enthesopathy, or sacroiliitis (as determined from radiography
of the pelvic region). We formally investigated prevalence of the
following articular signs and symptoms: arthralgia, stiffness,
swelling, ankylosis, paresthesia. Our working definition of
arthralgia was pain in any joint for more than 2 consecutive weeks
in the last year; joint stiffness was the lack of easy mobility of
a joint especially after periods of inactivity (for example,
sleeping or prolonged sitting), lasting for about 30 minutes or
more and improved with mild activity. Joint swelling was defined as
actual or referred persistent (more than 1 week) tumefaction of any
joints; and ankylosis as immobility and consolidation of a joint.
Paresthesia was a burning, prickling and/or tingling sensation in
one or more joints.
Measure of clinical severity of skin psoriasis
The Psoriasis Area and Severity Index (PASI) scores were calculated
using the formula originally proposed by Fredriksson et al. [18].
The clinical severity using the PASI was assessed during the first
hours of hospitalisation, before any medication was administered.
Body surface area (BSA) was measured using the palm or the rule of
nines methods. Plaque psoriasis was defined as localised when it
affected less than 10% and generalised when it involved more than
10% of the total BSA. Patients completed the self-administered PASI
(SAPASI). This is a structured, validated instrument measuring the
clinical severity of psoriasis based on the evaluation by the
patient himself of the affected area and average level of lesion
erythema, desquamation, and induration. SAPASI has been shown to
have an excellent acceptability by the patients and very close
correlation with PASI [19]. Information on socio-demographic
variables, clinical history, and other factors of clinical
interest, including gender, age, clinical type and location of the
disease, personal and family history of psoriasis and psoriatic
arthritis, smoking habits, and body mass index (BMI), was also
collected and recorded.
Statistical analysis
Differences in the prevalence of the considered symptoms observed
in the levels of each clinical and socio-demographic variable were
tested using chi-squared statistics. For PASI and SAPASI score
differences between the clinical types of psoriasis were tested
using the non-parametric Kruskal-Wallis test. All statistical
analyses were run under SPSS, version 9.0 for Windows [20].
Differences were considered significant when the P-value was <
0.05.
Results
During the study period, 1 721 patients with psoriasis were
hospitalised at our Institute. Of them, 269 were not contacted, 121
refused to participate, and 395 where excluded because they did not
meet the inclusion criteria. Thus, the total sample included 936
patients, but the clinical type was not recorded for 13 (1.4%) of
them. Among the 923 patients for whom the clinical classification
has been recorded, 455 (49.3%) were classified as having
generalised chronic plaque psoriasis; 147 (15.9%) had localised
plaque psoriasis; 118 (12.8%) had guttate psoriasis; 69 (7.5%) had
palmoplantar psoriasis; 29 (3.2%) had either localised or
generalised pustular psoriasis; 34 (3.8%) had other clinical types
(including inverse, erythrodermic). The remaining 71 patients
(7.7%) (95% confidence interval [C.I.] 6.0-9.5%) had PsA, according
to the ESSG diagnostic criteria. Of these 71 patients affected by
PsA, 66% presented generalised plaque psoriasis, 28% localised
plaque psoriasis and 5% pustular psoriasis of the palms and soles
(Barber), and 1% inverse psoriasis.
In table 1( Table 1 ), we compared
demographic and clinical characteristics of patients with PsA with
those of plaque psoriasis patients, subdivided into localised and
generalised. Prevalence of PsA was significantly higher in females
(9.4%, 95% C.I. 6.7-12.9) compared to males (6.6%, 95% C.I.
4.7-9.0). As for age groups, prevalence of PsA was lower in
patients less than 40 years old (5.2%, 95% C.I. 3.3-8.2) but then
similar in the other two age groups (9.2%, 95% C.I. 6.4-12.9 and
9.5%, 95% C.I. 6.1-14.3, among 40-59 and > 60 years old,
respectively). Frequency of positive family history for psoriasis
was approximately the same in PsA (49.3%) and generalised plaque
psoriasis (51.4%), with lower frequency in localised forms (36.1%).
A positive family history for PsA was more frequent in PsA than in
plaque psoriasis, but the difference was not statistically
significant. Frequency of smoking both during the study period and
at onset of disease was lower in PsA compared to plaque psoriasis
with P-values very near to the limit of statistical significance (p
= 0.056 and p = 0.066, respectively). No differences in BMI between
the three groups were noted. Median PASI score was 5.8 for
localised plaque psoriasis, 8.2 for generalised plaque psoriasis,
and 7.9 for PsA. Median SAPASI score was 7.9 for localised plaque
psoriasis, 14.9 for generalised plaque psoriasis, and 12.3 for PsA.
All patients enrolled received a topical therapy for psoriasis
during hospitalisation. The proportion of patients with a PASI
score > 10, requiring systemic treatment for psoriasis, was
24.1%. Almost 90% of patients with PsA received a specific
treatment for arthritis.
Overall 90.1% of patients with PsA referred arthralgia and 70.4%
stiffness, 67.7% referred or had joint swelling, 23.9% had
ankylosis and 25.4% referred paresthesia (table 2( Table 2 )).
Among patients with plaque psoriasis (i.e. either localised or
generalised type) and without PsA, 7.0% referred arthralgia, 4.2%
stiffness, 3.7% referred or had joint swelling, 1.2% had ankylosis
and 12.3% referred paresthesia. Differences between localised and
generalised plaque psoriasis were minimal and not statistically
significant. When considering the total number of patients
referring arthralgia (n = 106), 42 of them (39.6%) did not meet the
criteria for PsA. Among patients complaining of other joint signs
and symptoms, the proportion of patients with plaque psoriasis not
meeting the criteria for PsA was: stiffness 33.3%; swelling 31.4%;
ankylosis 29.2%; and paresthesia 80.4%.
Table 1 Characteristics of the study population
|
|
|
|
Psoriatic arthritis
|
|
|
|
n
|
%
|
n
|
%
|
n
|
%
|
P-value
|
|
Gender
|
Male
|
96
|
65.3
|
297
|
65.3
|
36
|
50.7
|
|
|
Female
|
51
|
34.7
|
158
|
34.7
|
35
|
49.3
|
0.005
|
|
Age
|
18-39 y
|
64
|
43.5
|
171
|
37.6
|
19
|
26.8
|
|
|
40-59 y
|
48
|
32.7
|
178
|
39.1
|
31
|
43.7
|
|
|
60+ y
|
35
|
23.8
|
106
|
23.3
|
21
|
29.6
|
0.169
|
|
Familial psoriasis
|
Yes
|
53
|
36.1
|
233
|
51.4
|
35
|
49.3
|
|
|
No
|
94
|
63.9
|
220
|
48.6
|
36
|
50.7
|
0.005
|
|
Familial PsA
|
Yes
|
35
|
23.8
|
108
|
23.8
|
23
|
32.4
|
|
|
No
|
112
|
76.2
|
345
|
76.2
|
48
|
67.6
|
0.287
|
|
Present smoker
|
Yes
|
81
|
55.9
|
227
|
50.3
|
26
|
38.2
|
|
|
No
|
64
|
44.1
|
224
|
49.7
|
42
|
61.8
|
0.056
|
|
Smoker at onset
|
Yes
|
89
|
61.0
|
256
|
56.8
|
30
|
44.1
|
|
|
No
|
57
|
39.0
|
195
|
43.2
|
38
|
55.9
|
0.066
|
|
BMI
|
<= 24.9
|
68
|
47.9
|
171
|
38.9
|
30
|
42.9
|
|
|
25-29.9
|
50
|
35.2
|
168
|
38.2
|
26
|
37.1
|
|
|
30+
|
24
|
16.9
|
101
|
23.0
|
14
|
20.0
|
0.363
|
|
Median PASI score
|
|
5.8
|
|
8.2
|
|
7.9
|
|
|
|
Median SAPASI score
|
|
7.9
|
|
14.9
|
|
12.3
|
|
|
Table 2 Prevalence (%) of articular symptoms and signs
in the study population
|
|
- Plaque,
- localised
- n = 147
|
- Plaque,
- generalised
- n = 455
|
|
|
|
Arthralgia
|
overall
|
7.6
|
6.8
|
90.1
|
15.8
|
|
hands
|
6.2
|
4.8
|
73.2
|
12.4
|
|
feet
|
2.1
|
2.4
|
60.6
|
8.5
|
|
sacrum
|
0.0
|
1.8
|
39.4
|
5.4
|
|
Stiffness
|
overall
|
3.4
|
4.4
|
70.4
|
11.2
|
|
hands
|
3.4
|
4.4
|
57.7
|
9.8
|
|
feet
|
1.4
|
1.1
|
32.4
|
4.5
|
|
Swelling
|
overall
|
3.4
|
3.7
|
67.6
|
10.4
|
|
hands
|
3.4
|
3.1
|
56.3
|
8.8
|
|
feet
|
1.4
|
1.8
|
35.2
|
5.2
|
|
Ankylosis
|
overall
|
0.7
|
1.3
|
23.9
|
3.6
|
|
hands
|
0.7
|
1.3
|
19.7
|
3.1
|
|
feet
|
0.0
|
0.2
|
5.6
|
0.7
|
|
Paresthesia
|
overall
|
9.5
|
13.2
|
25.4
|
13.7
|
Discussion
In this study we showed that in a single-centre research setting,
the prevalence of PsA diagnosed according to the ESSG criteria
among patients with psoriasis was 7.7%, with the true prevalence
very unlikely to be greater than 10%. On the other hand, joint
complaint (i.e. arthralgia, stiffness, swelling, ankylosis and
paresthesia) in our sample of patients with chronic plaque
psoriasis was as frequent as 17%. The prevalence of PsA in patients
with psoriasis has been reported to range greatly in different
studies from different countries. Similar prevalences were reported
by Shbeeb et al. (6.2%) and by Barisic-Drusko et al. who found that
7.2% of patients with psoriasis vulgaris were diagnosed as having
PsA [4, 6]. Zanolli et al. found the prevalence of PsA in their
population of 495 patients to be 17% and over 53% of psoriasis
patients to have a current or a previous history of arthralgia [7].
Biondi Oriente et al. reported that 21.3% of 646 patients with
psoriasis exhibited PsA [8]. Stern found that nearly 40% of 1 285
psoriasis patients suffered from arthralgia, and 20% had been
diagnosed as having PsA. Moreover, patients with PsA had more
extensive cutaneous disease and more frequently had a family
history of PsA [9]. Scarpa et al. found the prevalence of PsA in
his population of 180 psoriatic patients as being 34.4% [10].
Salvarani et al. compared the sensitivity and specificity of
existing criteria (i.e. Moll and Wright, ESSG, and Amor et al.
[21]) in a population of 205 psoriatic patients from Italy. Moll
and Wright criteria identified 22% of cases of PsA, ESSG criteria
24%, Amor criteria 24% and overall the 3 criteria identified 31% of
patients with PsA [5]. Our observed prevalence of PsA falls in the
lower portion of the range of previous estimates, but it is within
the range most commonly reported in the textbooks [13, 15, 22, 23],
and reviews [12-14]. Such large differences in the estimated
prevalence of PsA may be at least in part due to the different
research methods (e.g. different diagnostic criteria, questionnaire
versus physical examination, dermatological versus rheumatological
patient populations).
We showed that the joint signs and symptoms such as arthralgia,
stiffness, swelling, ankylosis and paresthesia are very frequent in
patients with PsA, but they are also quite common in patients with
plaque psoriasis not affected by arthritis. This could suggest that
the frequency of PsA could well be overestimated, both by
dermatologists and patients, if standardised diagnostic criteria
are not applied. It is interesting to note that approximately one
third of patients with specific articular signs and symptoms do not
have PsA. Thus, when dermatologists consider joint complaints in
patients with psoriasis, they have to distinguish PsA from other
causes of joint disease, such as rheumatoid arthritis,
osteoarthritis, gout, reactive arthritis, ankylosing spondylitis,
and inflammatory bowel disease related arthritis. These referred
joint complaints could be a disturbing factor in making a diagnosis
of PsA. There is still no specific diagnostic test for PsA, but the
ESSG classification criteria, Moll and Wright criteria, Amor et al.
criteria have been established to standardise the diagnosis of PsA.
The ESSG criteria which group PsA with other spondyloarthropathy
forms resulted in a sensitivity and a specificity of 87% [2]. The
ESSG diagnostic criteria are insensitive in disease of less than 1
year duration and cannot be used to diagnose some patients with an
early spondyloarthropathy, e.g. the patient who develops arthritis
before psoriatic skin lesions [24]. Whatever classification
criteria are applied, there is still no satisfactory definition of
PsA, and the criteria may be too specific and thus may fail to
represent the full spectrum of disease. The ESSG has developed a
set of criteria for the entire group of spondyloarthropathy
patients, with the specific intention of including patients with
undifferentiated spondyloarthropathy. The ESSG criteria are easy to
apply, and give higher priority to clinical than radiological
variables, being appropriate also for dermatologists.
There is an obvious need to distinguish patients with PsA from
patients with osteoarthritis or patients with psoriasis and joint
complaints not related to inflammatory arthritis. Moreover PsA
usually develops after skin disease, making the dermatologist the
physician who should recognise and treat early-phase PsA in order
to prevent the progression of the articular damage. Although plain
radiographs are the first line of imaging investigation,
dermatologists should be aware that they are often insensitive for
demonstrating the early changes of sacroiliitis, an important
feature for establishing the early diagnosis of seronegative
spondyloarthropathy. In contrast, MR imaging can demonstrate areas
that are undergoing active inflammatory changes and enthesitis,
supporting the diagnosis of PsA [25]. Ultrasonography has also
recently gained wider acceptance and popularity due to the ability
of this multiplanar technique to image both bone changes and soft
tissue abnormalities, including synovitis [26]. In conclusion,
patients with psoriasis referring joint symptoms need a close
follow up, either clinical or radiological, in order to detect
early changes of PsA, and start treatment that could limit
progression of PsA [27].
Acknowledgments
This Study was supported in part by funds from the Italian Ministry
of Health, Rome, Italy.
Appendix
The Italian Multipurpose Psoriasis Research on Vital Experiences
(IMPROVE) investigators who contributed to this study are: Gianluca
Antonelli, Simone Bolli, Rino Cavalieri, Massimo Luca Chinni,
Marcello Fazio, Nidia Melo Salcedo, Paola Moscatelli, Paolo Piazza,
Orietta Picconi, Maria Antonietta Pilla, Pietro Puddu, Giuseppe
Ruggiero, Francesco Sera, Romeo Simoni, Donatella Sordi.
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