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Joint Bone Spine 82 (2015) 267271

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Original article

Ultrasound study of entheses in psoriasis patients with or without


musculoskeletal symptoms: A prospective study
Emilie Acquacalda a,,1 , Christine Albert a,1 , Henri Montaudie b,1 , Eric Fontas d,1 ,
Agnes Danre a,1 , Christian Hubert Roux a,1 , Vronique Breuil a,1 , Jean Philippe Lacour b,1 ,
Thierry Passeron b,c,1 , Liana Euller Ziegler a,1
a

Department of Rheumatology, University Hospital of Nice, Nice, France


Department of Dermatology, University Hospital of Nice, Nice, France
c
Inserm, U1065, Centre Mditerranen de Mdecine Molculaire (C3M), team 12, Nice, France
d
Department of Clinical Research and Innovation, University Hospital of Nice, Nice, France
b

a r t i c l e

i n f o

Article history:
Accepted 19 January 2015
Available online 13 April 2015
Keywords:
Subclinical enthesitis
Psoriasis
Psoriatic arthritis
Ultrasonography
Biological therapies

a b s t r a c t
Objective: To estimate the prevalence of ultrasonographic enthesitis in psoriasis patients with or without
musculoskeletal symptoms and to investigate their evolution under systemic treatments given for the
cutaneous symptoms.
Patients and methods: Prospective bi-centre (rheumatology and dermatology) study over 6 months,
including psoriasis pts requiring systemic treatment, with or without musculoskeletal symptoms and/or
psoriatic arthritis (PsA). Clinical assessment (M0 and M6) included: BASDAI, HAQ, SPARCC, PASI and nail
disease. US assessment (M0 and M6) with Grey Scale and PD of 10 entheses was performed by one trained
rheumatologist blinded to clinical and biological data, scoring morphological, structural lesions and PD
signal.
Results: Complete data were obtained on 340 entheses in 34 patients. Twenty-two were asymptomatic
(PsO) and 12 symptomatic (PsA). They received conventional treatment and/or biologics.
At baseline: US abnormalities were found in 97.1% total population and in 86.4% PsO patients. 95/340
enthesitis were observed, 57/220 in PsO vs 38/120 in PsA (P = 0.258). Neither group had PD signal. Presence
of 24/90 enthesitis in patients with nail disease vs 33/130 without (P = 0.831).
At M6: Twenty-three patients were assessed. US morphological (thickness and hypoechogenicity) abnormalities were improved in PsO (n = 13) (P = 0.021) and PsA patients (n = 10) (P = 0.164) with a signicant
decrease of BASDAI, HAQ, SPARCC.
Conclusion: We observed a high frequency of US enthesitis in psoriasis patients, with or without musculoskeletal symptoms, requiring systemic treatment. At 6 months, US morphological abnormalities were
likely to improve. Further studies would be interesting to validate our data and to assess their potential
impact on PsA development.
2015 Socit francaise de rhumatologie. Published by Elsevier Masson SAS. All rights reserved.

1. Introduction
Enthesitis is a distinctive feature in the pathogenesis of spondyloarthritis (SA), group of diseases, including psoriatic arthritis (PsA)
[1,2]. PsA occurs in a variable percentage of psoriasis patients

Corresponding author. Department of Rheumatology, University Hospital of


Nice, 151, route de Saint-Antoine-de-Ginestire, 06200 Nice, France.
Tel.: +33 4 92 03 54 77; fax: +33 4 92 03 90 18.
E-mail address: acquacalda.e@chu-nice.fr (E. Acquacalda).
1
All authors approved the entirety of the submitted material and contributed
actively to the study.

that ranges from 10 to 30% depending on the studied population


[3]. Despite their clinical importance, entheseal abnormalities in
patients with SA are under-diagnosed and subclinical enthesitis
using ultrasonography (US) have been found mainly in lower limbs
of patients, including PsA patients. It has been demonstrated that
subclinical enthesitis is present in psoriasis patients without musculoskeletal involvement (PsO) compared with healthy controls
[48]. US is a sensitive technique and appears as a valid and reliable
tool for enthesitis evaluation [911]. In 2005, consensus denitions
of US elementary lesion, including enthesopathy, were published
by the OMERACT group [12,13]. Several studies have highlighted
the value of US in assessing inammation and the follow-up of
enthesis in SA [1420]. In fact, few longitudinal US studies have

http://dx.doi.org/10.1016/j.jbspin.2015.01.016
1297-319X/ 2015 Socit francaise de rhumatologie. Published by Elsevier Masson SAS. All rights reserved.

268

E. Acquacalda et al. / Joint Bone Spine 82 (2015) 267271

evaluated the response to therapy of entheseal abnormalities in


SA but none in PsA [14,15]. Some US scoring systems were used
both for diagnostic and for assessing changes under treatment
[1618,21], nevertheless their performances varied according to
the purpose.
Our study aimed to investigate the prevalence of enthesitis with
Power Doppler Ultrasonography (PDUS) in psoriasis patients without articular symptoms (PsO) and in patients with PsA, and to assess
their evolution under systemic treatment. In addition, as clinical
and imaging observations suggest that there may be a link between
systemic enthesopathy and psoriatic nail disease, we planned to
investigate if nail disease in psoriasis is linked to a greater degree of
enthesitis compared with psoriasis patients without nail disease.
2. Methods
2.1. Patients groups and clinical assessment
PsO patients requiring systemic treatment, and PsA were
prospectively recruited in 2 French departments of Rheumatology
and Dermatology (University hospital of Nice, France) from January
2011 to June 2012. Inclusion criteria were age over 18 years and
a diagnosis of psoriasis without or with articular symptoms (PsA
patients being dened by the CASPAR criteria) requiring systemic
treatment. The patients were included before the introduction
of the rst systemic treatment (i.e. methotrexate, cyclosporine
and acitretin) or biologic therapies (iniximab, adalimumab, etanercept and ustekinumab). Exclusion criteria were a history of
inammatory musculoskeletal disease except PsA, a chronic infectious disease or a cancer. Informed consent was obtained from all
patients before study enrolment.
Patients underwent a clinical and laboratory evaluation at baseline, and after 3 and 6 months of treatment. PDUS evaluation was
performed at baseline and after 6 months. Clinical and laboratory
assessment were realized by a trained rheumatologist and dermatologist blinded to ultrasound data. The following data were
recorded for each patient at the rst visit: age, sex, osteoarticular
and dermatological symptom duration, psoriatic nail involvement,
disease modifying anti rheumatic drugs (DMARD), biologic therapy received for PsA or psoriasis; C-reactive protein (CRP) level
(normal 05 mg/L), erythrocyte sedimentation rate (ESR) level
(normal 515 mm/h), HLA B27 status and CCP antibodies. Therapeutic decision was taken independently of the PDUS ndings by
the dermatologist or the rheumatologist of the patient in real life
conditions.
At each visit, psoriasis severity was scored using the psoriasis
area and severity index (PASI) and the body surface area (BSA) measurement. The impact of the disease on quality of life was assessed
by the Dermatology Life Quality Index (DLQI). Rheumatologic evaluation included: tender and swollen joint count, tenderness of
16 entheses (Spondyloarthritis Research Consortium of Canada,
SPARCC), the Bath Ankylosing Spondylitis Disease Activity Index
(BASDAI) and the Functional Index (HAQ = Health Assessment
Questionnaire). Data on serum markers of inammation C-reactive
protein (CRP) and ESR were recorded at each clinical visit.
2.2. Ultrasonography
US examinations were performed at the Rheumatology
department of the University Hospital (Nice, France) by one
rheumatologist experienced in this technique, using a MyLab 70
XVG Esaote (Saint-Germain-en-Laye, France) equipped with multifrequency linear array transducers (6 to 18 MHz).
The rheumatologist performing the US examination was
unaware of the clinical and laboratory ndings, and was not

involved in the treatment decisions. US examination was performed in a darkened room. The patients were asked not to discuss
their clinical symptoms to avoid the possibility of bias. In each
patient, 5 entheses were scanned bilaterally with a systematic
longitudinal and transverse PDUS examination: Achilles tendon,
plantar fascia insertion, quadriceps insertion, patellar proximal and
brachial triceps tendon insertion. Entheses with previous surgical
procedures were not evaluated. Power Doppler (PD) assessment
was performed at the bony margins and entheseal site with a
Doppler frequency of 8.3 MHz. Pulse repetition frequency of 500 Hz
was adjusted to the lowest permissible value to maximize sensitivity. A low-wall lter was used. Flow was additionally demonstrated
in 2 planes and conrmed by pulse wave Doppler spectrum to
exclude artefacts.
Patients were placed in a supine decubitus position to assess
entheses of knee (quadriceps tendon insertion and patella ligament origin) exed at 45 for gray scale (GS) and power doppler
(PD); to assess the entheses of feet (Achilles tendon and plantar aponeurosis): prone decubitus with the feet hanging outside
the examination table in slight at 90 dorsal of exion for GS
and in neutral position for PD; to assess brachial triceps enthese:
sitting facing the examiner with armed exed at 90 and palmar surfaces on a table. US enthesitis were identied according
to the outcome measures in rheumatoid arthritis clinical trials
(OMERACT) denition: abnormally hypoechogenicity (loss of normal brillar architecture) and/or thickened tendon or ligament at
its bone attachment (may occasionally contain hyperechogenicity
foci consistent with calcication), seen in two perpendicular planes,
which may exhibit Doppler signal and/or bony changes, including
enthesophytes, erosions or irregularity [12]. The following elementary lesions were assessed for each enthesis with a binary score
(presence/absence): morphological (i.e. hypoechogenecity and/or
thickening at the body of the tendon) and structural abnormalities
(entheseal calcic deposits, bone erosion and/or enthesophytes) in
GS and intra-enthesis PD signals at the cortical bone insertion. We
took as reference value the tendinous thicknesses used in the MASEI
score [22].
2.3. Statistical analysis
Categorical data are expressed as frequencies, and continuous
variables are given as means (SD). The Wilcoxon signed-rank test
was used to compare changes in clinical and functional scores, from
baseline to the end of the study (M6). The rates of overall and
individual lesions by ultrasound in PsO and PsA patients and in subgroups with or without nail disease were compared by using a 2
test. Changes in US morphological abnormalities between baseline
and M6 were studied using the Mc Nemars test for paired binary
data. All tests were two sided and the signicance level was set to
5%. We used SPSS software, version 11.0 (Chicago, IL, USA) for the
statistical analyses.
3. Results
3.1. Patients characteristics
PDUS were performed on 34 patients (Table 1) who were starting a rst systemic therapy with methotrexate (MTX) (n = 23, 67.6%)
or biologic therapy (n = 11, 32.4%), (etanercept, iniximab, ustekinumab, and adalimumab).
We included:
22 PsO patients: 19 starting conventional systemic treatment
(MTX) and 5 biologics (iniximab n = 1, adalimumab n = 1, ustekinumab n = 3);

E. Acquacalda et al. / Joint Bone Spine 82 (2015) 267271


Table 1
Baseline characteristics of the population in PsO and PsA patients.
Total patients (n)
Age, mean (years)

US found at least one sign of enthesitis in 102/220 (46.4%) entheses


in PsO patients and in 65/120 (54.2%) in PsA patients (P = 0.169).
In total population, we found the highest number of enthesitis
in Achilles tendon (45/340, 13.2%) and in brachial triceps tendon
(35/340, 10.3%). In PsO patients, Achilles tendon was the most
affected enthesis (30/220, 13.6%) whereas in PsA patients, it was the
brachial triceps tendon (16/120, 13.3%). Hypoechogenicity lesions
were detected in 27/220 (12.3%) entheses in PsO patients in 26/120
(21.7%) entheses in PsA patients (P = 0.022). There were no signicant differences between PsO and PsA concerning the other lesions
and notably structural abnormalities.
Patients with nail disease had 44/90 (48.9%) enthesitis compared to 58/130 (44.6%), (P = 0.532) in patients without nail disease.
The overall frequency of each elementary lesion at each enthesis
at baseline is shown in Table 2.

34 (20 M; 14 W)
43.45 12.3

Patients (n)
Disease duration, mean (years)
Nail disease (n)
BSA (%)
PASI
DLQI
BASDAI
SPARCC
HAQ
Mean CRP (mg/L)
Treatments
Methotrexate (n)
Biologics (n)

PsO

PsA

22
16.7 9.7
9
5 22.9
15.8 9.9
9.8 3.9
NA
NA
NA
4.25

12
14.4 6
8

269

46.4 16.7
6.73 2.6
1.1 0.5

23 (67.6%)
11 (32.4%)

3.4. Evolution of enthesitis under systemic treatment

NA: not applicable.

12 PsA patients: 10 PsO patients fullling to the CASPAR criteria


after evaluation by a rheumatologist during the study because of
osteoarticular symptoms. The 2 others patients were PsA patients
addressed by rheumatology department. All of them presented
cutaneous disease. Six were starting conventional systemic treatment (MTX) and 6 biologics (etanercept n = 4, iniximab n = 2).
The mean symptoms duration was 16.7 years ( 9.7) for psoriasis and 14.4 years ( 6) for the PsA. The clinical presentation of the
cutaneous lesions was: psoriasis vulgaris (60%, 29 patients), psoriasis guttate (4.7%, 2 patients), generalized psoriasis (2.3%, 1 patient),
nail psoriasis only (2.3%, 1 patient) and palmo-plantar psoriasis
(2.3%, 1 patient). Nail disease was seen in 17 patients: PsO (n = 9) and
PsA (n = 8). Among 12 PsA patients, 3 patients had an axial involvement, 3 patients a peripheric including enthesitic involvement and
6 patients both. None extra articular manifestation was nded.
3.2. Disease activity and functional course in PsO and PsA
At baseline, mean BASDAI, SPARCC and HAQ scores were respectively 46.4 ( 16.7), 6.73 ( 2.6), 1.1 ( 0.5). A signicant decrease
of mean BASDAI, SPARCC and HAQ was found after 6 months of
treatment (P < 0.0001 for each score).
The mean PASI, SCA and DLQI scores, were respectively at baseline to 15.8 ( 9.9), 30. 47 ( 22.6) and 9.8 ( 3.9) and decreased
signicantly at M6, to 5.4 ( 6.4, P < 0.0001), 8.2 ( 10.4, P < 0.0001)
and 2.1 ( 2.2, P < 0.0001).
3.3. PDUS abnormalities in Ps0 and PsA patients
We evaluated a total of 340 enthesis. At baseline, at least one
entheseal abnormality was observed in 97.1% of the total population and in 86.4% of PsO patients. No PD signal was detected. GS

At 6 month, 23 patients were assessed receiving MTX (n = 12)


alone or associated with biologics (n = 11) (Table 3). Eleven patients
refused ultrasonography study. US morphological abnormalities
(hypoechogenicity and thickness) were improved both in PsO
patients (n = 13) and PsA patients (n = 10). PsO patients had signicant improvement of US morphological abnormalities with 39/130
(30%) enthesitis at baseline compared to 23/130 (17.7%) at M6
(P = 0.021). In PsA patients, PDUS changes after treatment showed a
no signicant improvement from baseline to M6, with respectively
33/100 (33%) enthesitis and 24/100 (24%) (P = 0.164). At M6, the
analysis of enthesitis on the basis of the treatment groups showed
in PsO patients: a signicant decrease with MTX alone [M0: 23/80
(28.8%) and M6: 12/80 (15%) (P = 0.035)] and a improvement with
biologics alone [M0: 16/80 (32%) and M6: 11/80 (22%) (P = 0.359)].
We did not realize study of correlation between the ultrasound data
and the clinical evaluation as well as the score SPARCC.
4. Discussion
In the present study, we found US enthesitis (46.4%) in a high
percentage of PsO patients without rheumatologic symptoms compared with the previous studies. These results can be explained by
the inclusion of only PsO patients requiring systemic treatment.
Gisondi et al. studied US entheseal abnormalities in the lower limbs
of 30 PsA patients without articular involvement and 30 controls;
they found signicantly more US signs of enthesopathy (32.9%)
and higher mean GUESS score in PsO patients as compared with
controls [23]. De Filippis et al. reported that 6 of 24 PsO patients
(25%) showed asymptomatic US abnormalities in hand entheses
and tendon [24]. Gutierrez et al. found signicantly more US signs
of enthesopathy and higher GUESS score in the lower limbs of 45
psoriasis patients (32.9%) as compared with 45 healthy controls
(8.4%) [8]. In the study by Naredo et al., in a total of 162 patients
with PsO and 60 controls, the percentage of entheses with a least
one US sign of enthesopathy were signicantly more important

Table 2
Baseline PDUS ndings in PsO and PsA patients.

Hypoechogenicity
Thickening
Erosion
Calcication
Power Doppler
Morphological lesions
Structural lesions
All lesion

Total population (340 entheses)

PsO (220 entheses)

PsA (120 entheses)


%

P values

53
69
46
98
0
95
116
167

15.6
20.3
13.5
28.8
0
27.9
34.1
49.1

27
43
26
57
0
57
69
102

12.3
19.5
11.8
25.9
0
25.9
31.4
46.4

26
26
20
41
0
38
47
65

21.7
21.7
16.7
34.2
0
31.7
39.2
54.2

0.022
0.642
0.212
0.108

0.258
0.147
0.169

270

E. Acquacalda et al. / Joint Bone Spine 82 (2015) 267271

Table 3
Ultrasonography morphological lesion from baseline to 6 months.
M0

Total population
PsO
PsA

M6

P values

Enthesitis

Total enthese

Enthesitis

Total enthese

72
39
46

230
130
100

31.3
30
33

47
23
24

230
130
100

20.4
17.7
24

in psoriasis group (11.6%) than in controls (5.3%) [6]. Besides,


in accordance with previous studies, we found more frequently
Achilles enthesis in PsO patients [6,8].
In our PsA population, prevalence of US enthesitis was 54.2%
with no signicant differences in analysis of each elementary lesion.
We found more frequent hypoechogenicity in PsA patients than
in PsO patients with a statistically signicant difference. Balint
et al. studied seven patients with PsA in a cohort of 35 SA patients
with mean disease duration of 24.9 years; they showed that 22% of
entheses assessed were abnormal on clinical examination and 56%
were abnormal on grey scale ultrasound [16]. Freeston et al. showed
ultrasound entheseal abnormality in 24 (8.1%) of 296 entheses in
18 (42.9%) early PsA patients compared to 9 (11.5%) of 78 entheses
in 3 (30%) controls [25]. We found more frequently brachial triceps
tendon enthesis. According to the mean BMI, we expected to nd
more of enthesis on lower limbs; moreover, a recent study shows
that obesity is correlated with a majority of Achilles enthesis [26].
In our study, we did not nd PD signal entheseal in PsO and PsA
patients contrary to previous studies, however, their percentages of
PD were rather low [6,8]. Naredo et al. showed entheseal PD signal
present in 10 (7.4%) psoriasis patients, whereas no controls showed
this nding [6]. In the study of Ash et al., in a total of 372 entheses
in PsA patients with nail disease compared with 180 entheses in
patients without nail disease, PD signal was present respectively in
3/72 (1%) and 2/180 (1%) entheses [7]. We suggest that the hyperkeratosis, the obesity and the overweight condition in severe PsO
and Psa patients could be factors limiting detection of PD signal.
The tendons examined by US were assessed in a neutral but
not fully relaxed position, and this may reduce the sensitivity of
PD, potentially reducing signal by compressing vessels [27]. Unfortunately, no consensus US denition on elementary lesion and
standardization of exam are established, but there are necessary
to improve the quality of studies and the value of US in enthesitis.
The rate of US enthesitis was moderate and not signicantly
different in patients with (26.7%) or without (25.4%) nails disease.
Ash et al. showed that patients with nail disease had higher total
ultrasound scores and a correlation between severity of nail disease
and ultrasound inammation and chronic lesion [7].
To the best of our knowledge, this is the rst study evaluating
the evolution of US abnormalities in subclinical enthesitis of PsO
patients under systemic treatment. Morphological abnormalities
(thickeness and hypoechogenicity) demonstrated a highly significant improvement from baseline as compared to 6 months after
the introduction of the systemic treatment (methotrexate or biologics). Naredo et al. have demonstrated a good response of entheseal
morphological abnormalities, PD signal and bursitis with anti TNF
therapy for 6 months in 197 patients with SA [13]. Aydin et al.
showed a signicant improvement of subclinical Achilles enthesitis
in SA patients after 2 months of anti TNF therapy [12]. Reduction
in GS score correlated with CRP changes and PD score reduction
correlated with ESR reduction.
Here, we showed that subclinical enthesitis of both PsO and
PsA population improve under systemic treatment. Both patients
under methotrexate and biologics had a reduction of the enthesitis
at US examination. The relative small number of patients studied
in this pilot study prevents drawing denitive conclusion on the
relative effectiveness on subclinical enthesitis of these two types of

0.006
0.021
0.164

treatment. Enthesitis is known to be the central involvement of PsA;


however, data concerning the subclinical enthesitis detected with
US are recent and remain limited. Our results conrm a high prevalence of subclinical enthesitis in PsO requiring systemic treatment.
This study also shows for the rst time that these asymptomatic
enthesitis signicantly improve under systemic treatment given
for the skin involvement. The main question is the signicance of
these subclinical enthesitis. Long-term follow-up studies of PsO
patients with and without subclinical enthesitis are warranted to
determine if they have a predictive value of future PsA, and to determine if rapid introduction of a systemic treatment could impact
this evolution. However, our results must be interpreted with
caution because of the low size of our heterogeneous population.

Disclosure of interest
The authors declare that they have no conicts of interest concerning this article.

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