Rheumatology 2013;52:510–514
doi:10.1093/rheumatology/kes306
Advance Access publication 21 November 2012
RHEUMATOLOGY
Original article
Validation in Spanish of a screening questionnaire
for the detection of psoriatic arthritis in patients
with psoriasis
Leandro G. Ferreyra Garrott1, Enrique R. Soriano1, Javier E. Rosa1,
David A. Navarta1, Carla Saucedo1, Marina Scolnik1, Zaida Bedran1,
Mirtha Sabelli1, Maria V. Garcı́a1, Carolina Anselmi2, Ricardo Galimberti2,
Luis J. Catoggio1, M. Elaine Husni3 and Abrar A. Qureshi4
Abstract
Objective. A patient self-administered questionnaire [PsA Screening and Evaluation (PASE)] has been
developed and validated in English, but has not been tried in Spanish speaking populations. This study
aimed to adapt and validate PASE in Spanish to screen Spanish speaking psoriasis patients for signs and
symptoms of inflammatory arthritis.
CLINICAL
SCIENCE
Methods. Initial translation from English to Spanish (forward translation) was performed by two independent translators and the resulting versions were synthesized during a consensus meeting. The questionnaire
was tried in a pilot study and resulted in a change in the agreement scale for a frequency scale with
wording adaptation [Spanish PASE (PASE-S)].
Results. One hundred and eleven patients were screened with PASE-S; 25 with PsA (without previous
treatments), 23 with psoriasis, 22 with psoriasis and OA and 41 with OA without psoriasis. The diagnosis
of psoriasis was performed by a dermatologist, and a rheumatologist determined the diagnosis of PsA or
OA. Patients with PsA had statistically significant higher symptoms, function and total PASE-S scores
compared with those without PsA. Receiver operator curves showed an area under the curve of 0.79 (95%
CI 0.69, 0.89) for the total score. A cut-off value 534 showed sensitivity of 76%, and specificity of 74.4%
for the diagnosis of PsA.
Conclusion. The validated PASE questionnaire is a self-administered tool that can be used to screen for
PsA among patients with psoriasis in a Spanish speaking population. PASE was able to distinguish
between symptoms of PsA and OA.
Key words: psoriasis, psoriatic arthritis, screening questionnaire, PASE.
1
Sección Reumatologı́a, Servicio de Clı́nica Médica, Hospital Italiano
de Buenos Aires, Instituto Universitario, Escuela de Medicina, Hospital
Italiano de Buenos Aires, Fundación Dr Pedro M. Catoggio para el
Progreso de la Reumatologı́a, Ciudad Autonoma de Buenos Aires,
Argentina, 2Servicio de Dermatologı́a, Hospital Italiano de Buenos
Aires, Ciudad Autonoma de Buenos Aires, Argentina, 3Departments of
Rheumatic and Immunologic Diseases, Cleveland Clinic Foundation
Cleveland, Ohio, USA and 4Department of Dermatology and the Center
for Skin and Related Musculoskeletal Diseases, Brigham and
Women’s Hospital, Harvard Medical School, Boston, Massachusetts,
USA.
Submitted 8 March 2012; revised version accepted
26 September 2012.
Correspondence to: Enrique R. Soriano, Sección Reumatologia,
Servicio de Clı́nica Médica, Hospital Italiano de Buenos Aires,
Gascon 450 (1181), Ciudad Autónoma de Buenos Aires, Argentina.
E-mail: [email protected]
Introduction
Between 6% and 42% of patients with psoriasis have PsA
[1–6]. The prevalence of PsA varies between 0.04 and
0.74% according to different studies in different countries
[5, 7–9]. Because psoriasis skin lesions usually precede
the onset of joint symptoms by 10 years [7] dermatologists
are in an ideal position to screen individuals for PsA early
in the course of their disease. In recent years, different
groups have developed self-administered questionnaires
for the detection of PsA in the general population and in
patients with psoriasis [10–15]. Husni and Qureshi
described and validated the PsA Screening and
! The Author 2012. Published by Oxford University Press on behalf of the British Society for Rheumatology. All rights reserved. For Permissions, please email: [email protected]
Spanish tool for diagnosis of PsA
Evaluation (PASE) questionnaire for the diagnosis of
inflammatory joint disease in patients with psoriasis
[12, 13, 15]. The PASE was designed to help dermatologists identify individuals with psoriasis who would benefit
from a prompt referral to rheumatologists. PASE consists
of 15 questions divided into two subscales: symptoms
subscale with seven questions and function subscale
with eight questions. The scoring system provides a
numeric scale; those individuals who are more likely to
have PsA will score higher than individuals without PsA
[12, 13, 15].
There are no validated screening tools in Spanish to be
used in Argentina for the assessment of patients with
psoriasis, so we sought to validate the PASE to help
dermatologists to identify patients at higher risk of
having early PsA. The objective of this study was to translate into Spanish and validate the PASE questionnaire for
the detection of PsA in patients with psoriasis.
Patients and methods
Institutional review board approval was obtained from the
Comite de Etica de Protocolos de Investigacion, and all
patients signed an informed consent.
Cross-cultural validation
The questionnaire is already validated in English [12, 13,
15]. It was translated into Spanish by two independent
bilingual physicians who were familiar with the use of
the questionnaire. Subsequently, one experienced
rheumatologist, with knowledge of the purpose of the
study, examined semantic, idiomatic and conceptually
translated the questionnaires and produced a single version. Retranslation into English was made by another bilingual physician who was unaware of the study and the
original questionnaire in English. Both English versions
were compared (original and retranslated), and as they
were very similar the Spanish version was implemented
in a pilot study involving six patients. As a result of this
pilot study many patients referred difficulties with the
interpretation of the original agreement scale (strongly
agree—strongly disagree). We therefore chose to
change the rating scale to a frequency scale (never,
almost never, do not know, almost always, always) with
wording adaptation. This new questionnaire was accepted and easily understood by two of the six patients
in the pilot study and was then adopted (the translated
PASE questionnaire is available as supplementary data,
available at Rheumatology Online).
Study population
This was a cross-sectional study. Adults >18 years of age
who were able to read and understand Spanish were eligible for the study. The gold standard for diagnosis of
psoriasis and PsA was based on a clinical evaluation by
a dermatologist and a rheumatologist, respectively. The
diagnosis of OA was based on the clinical and radiographic evaluation by a rheumatologist. The diagnosis of
PsA was based on the CASPAR [16] criteria.
www.rheumatology.oxfordjournals.org
Recruitment took place at the Hospital Italiano de
Buenos Aires (HIBA) Dermatology and Rheumatology outpatients’ clinics. Four groups of patients were included:
group 1 were patients with PsA without treatment with
DMARDs followed at the HIBA rheumatology outpatient
clinic; group 2 were patients with psoriasis without PsA
(after evaluation by rheumatologists in the study), followed
at the HIBA Dermatology outpatient clinic; group 3 were
patients with psoriasis and OA followed at any or both of
the outpatient clinics; and group 4 were patients with OA
without psoriasis followed at the HIBA Rheumatology
clinic. The two latter groups were included because of
the involvement of the DIP joints, which usually poses
difficulties in the differential diagnosis with PsA.
Clinical assessment
All patients were assessed by dermatologists (C.A., R.G.)
and rheumatologists (L.G.F.G., E.R.S., J.E.R., D.A.N.) for
psoriasis and PsA/OA-definitive diagnosis The following
data were recorded in all PsA patients: disease duration,
type of arthritis onset (monoarticular, oligoarticular or
polyarticular), all assessments recommended by
GRAPPA and OMERACT [17]: 66/68 painful and swollen
joints, visual analogue scale disease activity by physician
and patient, assessment of functional capacity (HAQ [18]),
evaluation of the axial involvement (BASDAI–BASFI)
[19–21], presence of enthesitis, dactylitis. Extension of
the skin using the Psoriasis Area Severity Index (PASI)
[22, 23] was assessed in all patients with psoriasis. In
those in whom it was justified, radiological and laboratory
studies were conducted to better assess patients’ diagnosis. All cases of PsA included had never received
DMARD therapy.
Statistical analysis
Only patients with complete data were included.
Continuous measures were summarized by mean and
S.D., or by median and interquartile range where appropriate; categorical measures were summarized by per cent
and 95% CIs. Wilcoxon rank-sum tests were used to test
for differences between the PsA and non-PsA groups for
total, function and symptom scores. Receiver operator
curves (ROCs) were used to evaluate the discriminative
value and to pick the best cut-point for total PASE score
to predict PsA. Ninety-five per cent exact binomial CIs
were constructed for both sensitivity and specificity. A
sensitivity or specificity of 50% indicates that the criteria
used for classification does not distinguish between
groups better than chance; therefore, if the 95% CIs do
not overlap 50%, we can conclude that our score does
better than chance assignment at the 0.05 significance
level.
Results
One hundred and eleven patients were included:
25 patients with PsA (group 1); 23 patients with psoriasis
without arthritis (group 2); 22 patients with psoriasis
and OA (group 3); and 41 patients with OA without
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Leandro G. Ferreyra Garrott et al.
TABLE 1 Characteristics of study population
Patient characteristic
PsA
Psoriasis
Psoriasis + OA
OA alone
Total
n
Age, mean (S.D.), years
Psoriasis duration, mean (S.D.), years
Articular involvement duration, mean (S.D.), years
Articular involvement, n (%)
Monoarthritis
Oligoarthritis
Polyarthritis
Enthesitis alone
DAS28, mean (S.D.)
BASDAI, mean (S.D.)
BASFI, mean (S.D.)
HAQ, mean (S.D.)
PASI, mean (S.D.)
25
48.6 (10.5)
15.4 (11.8)
4.2 (4.7)
23
47.9 (12.8)
17.4 (19.7)
—
22
66.9 (10.7)
18.3 (12.9)
11.7 (8.3)
41
61.7 (11.1)
—
10.6 (8.4)
111
56.9 (13.6)
—
5 (20)
14 (56)
4 (16)
2 (8)
3.8 (1.3)
4.5 (2.5)
2.5 (2.2)
0.67 (0.53)
2.6 (3.8)
6.5 (6.8)
1.6 (1.3)
—
—
TABLE 2 PASE-S symptom, function and total scores of study population
PASE-S score
PsA (n = 25)
Psoriasis
(n = 23)
P-valuea
PsA + OA
(n = 22)
P-valuea
(vs PsA)
OA (n = 41)
P-valuea
(vs PsA)
Symptom score, mean (S.D.)
Function score, mean (S.D.)
Total score, mean (S.D.)
Total score, median (IQR)
22.5 (6.4)
21.1 (8.39)
43.3 (13.6)
43 (34–52)
13.3 (4.6)
12.8 (7)
26.1 (10.7)
24 (19–30)
<0.0001
0.0006
<0.0001
<0.0001b
16.6 (6.4)
17.2 (7)
33.9 (12.8)
32 (23–41)
0.0042
0.0876
0.043
0.0159b
15.4 (5.6)
13.7 (6.4)
9 (10.3)
29 (20–35)
0.0001
0.0010
0.0001
0.0001b
IQR: interquartile range. aStudent’s t-test; bMann–Whitney U-test.
psoriasis (group 4). Demographic characteristics are summarized in Table 1.
There was a statistically significant difference between
the scores of patients with PsA compared with those without PsA (Table 2). Patients with PsA had significantly
higher symptom, function and total scores compared
with all the other groups.
Fig. 1 presents the ROCs for discrimination of PsA of
the PASE-S symptoms, function and total scores, which
had an area under the curve of 0.81 (95% CI 0.71, 0.90);
0.73 (95% CI 0.61, 0.85) and 0.79 (95% CI 0.69, 0.89),
respectively. There were no differences in mean total
PASE-S score among males and females except in patients with OA alone, where the three males had significantly lower PASE-S scores [mean total score: 16.7 (S.D.
1.1) vs 30 (S.D. 10); P = 0.0281) than females.
The total PASE-S scores ranged from 15 to 69, and a
total PASE score of 34 was determined to be the optimal
cut-point for distinguishing PsA from non-PsA in all participants. At this cut-point, sensitivity was 76% (95% CI
55%, 90%) and specificity was 74% (95% CI 64%, 83%).
A value 526 showed 92% sensitivity and 48% specificity,
and a cut-point value of 47 had 91% specificity and 36%
sensitivity.
Forty-three patients were referred from the Dermatology outpatient clinic (all 23 patients with psoriasis alone,
512
13 of the 22 patients with psoriasis and OA and 7 finally
diagnosed as PsA). PsA was diagnosed by the rheumatologists in 7 (19%) of them. Five of these seven patients
had a PASE score >34 (sensitivity 71%). Among this subgroup of patients referred from Dermatology, another
seven patients had a PASE score of >34 without PsA
(specificity 84%).
Discussion
Skin involvement in psoriasis usually precedes articular
involvement, and dermatologists usually are seeing
these patients before any other specialist. In many settings it is often not possible for a rheumatologist to
review all patients with psoriasis looking for PsA. Early
diagnosis of PsA is very important nowadays, as early
treatment will improve articular prognosis. Therefore, a
screening questionnaire would be helpful for screening
large number of subjects with psoriasis to identify probable cases with PsA and their referral to a rheumatologist.
Several questionnaires have been developed and tried
with variable results, such as the ToPAS (the Toronto
Psoriatic Arthritis Screen) [14]. This was aimed for the
general population, and not just for patients with psoriasis,
and showed high sensitivity and specificity for the diagnosis of PsA in all groups of patients in whom it was
www.rheumatology.oxfordjournals.org
Spanish tool for diagnosis of PsA
FIG. 1 ROCs for PASE-S: total, symptom and function scores.
tested. ToPAS differs from previous questionnaires in that
it includes pictures of psoriasis and nail lesions [14] The
Psoriasis and Arthritis Questionnaire (PAQ), only presented in abstract form, was subsequently modified and
validated by Alenius et al. [10] (mPAQ). Ibrahim et al. [6]
developed the PEST (Psoriasis Epidemiology Screening
Tool) in England for the diagnosis of PsA in people with
psoriasis with adequate sensitivity and specificity.
PASE was developed for the detection of inflammatory
joint disease in patients with psoriasis at the Center for
Skin and Related Musculoskeletal Diseases Clinic, a combined dermatology–rheumatology clinic at Brigham and
Women’s Hospital in Boston [15]. The authors showed
that the PASE was able to differentiate patients with PsA
from those without PsA. A total PASE score of 47 was
determined to be the optimal cut-point for distinguishing
PsA from non-PsA with 82% sensitivity and 73% specificity. In a later, larger validation study with 190 patients
they found that a cut-point of 44 had 76% (95% CI
59%, 88%] sensitivity and 76% (95% CI 68%, 82%) specificity [13].
In addition, a subgroup showed excellent reliability
test–retest correlation coefficients that ranged from 0.35
to 0.80. Response to treatment was assessed in the PsA
group, post-treatment PASE scores were significantly
lower than pre-treatment scores (P = 0.034) [13].
We chose the PASE questionnaire because it had been
validated in a large number of patients arising from a combined Dermatology–Rheumatology clinic. In this study, we
www.rheumatology.oxfordjournals.org
were able to show that PASE-S, a self-administered tool
was useful to discriminate patients with PsA from those
without PsA including patients with OA.
Because of comprehension problems during the pilot
testing of the translated questionnaire, we changed the
type of scale (from agreement to frequency), and that
might explain lower general scores and lower cut-off
value in our study. However, our results showed similar
sensitivity and specificity to that shown in the original developing and validation studies [13, 15]. As PASE is a
continuous scale according to different needs different
cut-off values could be chosen. For example, if there is
a large rheumatology clinic to refer patients to, a lower
cut-off value with higher sensitivity could be chosen, on
the other hand if rheumatologists are scarce with large
waiting lists a higher PASE value with higher specificity
could be chosen.
In summary, we performed a cross-cultural validation of
a screening questionnaire for PsA in patients with psoriasis. This should prove useful for the detection of PsA in
patients with psoriasis in Spanish-speaking countries.
Rheumatology key messages
The PASE is valid for the diagnosis of PsA in
Spanish-speaking patients with psoriasis.
. PASE was able to discriminate between psoriasis
patients with PsA and OA.
.
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Leandro G. Ferreyra Garrott et al.
Acknowledgements
The PASE questionnaire is licensed to Pfizer and Merck.
Funding: This work was supported by an Institutional
Grant from Hospital Italiano de Buenos Aires.
Disclosure statement: A.A.Q. has been a consultant for
Abbott, Novartis, the US Centers for Disease Control
and Prevention and Janssen, and has received a grant
from Amgen. All other authors have declared no conflicts
of interest.
Supplementary data
Supplementary data are available at Rheumatology
Online.
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