Musculoskeletal ultrasonography of the Achilles tendon and plantar fascia in spondyloarthritis patients

The Egyptian Rheumatologist xxx (xxxx) xxx–xxx

Contents lists available at ScienceDirect

The Egyptian Rheumatologist journal homepage: www.elsevier.com/locate/erhe

Original Article

Musculoskeletal ultrasonography of the Achilles tendon and plantar fascia in spondyloarthritis patients ⁎

Khadija Baccouchea, , Linda Mania, Nejla Elamria, Neila Fathallahb, Hounaida Zaghouanic, Safaa Belghalia, Hela Zeglaouia, Elyes Bouajinaa a

Rheumatology Department, Farhat Hached Hospital, Faculty of Medicine, Sousse University, Sousse, Tunisia Pharmacology Department, Faculty of Medicine, Sousse University, Ibn El Jazzar, Sousse, Tunisia c Radiology Department, Farhat Hached Hospital, Faculty of Medicine, Sousse University, Sousse, Tunisia b

A R T I C L E I N F O

A B S T R A C T

Keywords: Enthesis Spondyloarthritis Mechanical low back pain Ultrasonography Power doppler

Aim of the work: To assess the frequency and severity of peripheral enthesitis in spondyloarthritis (SpA) patients using musculoskeletal ultrasound (MSKUS) in B mode associated with power Doppler (PD) compared to a group of patients with mechanical low back pain (M-LBP). Patients and methods: The study included 40 SpA patients and 20 M-LBP patients as a control group. Ultrasound (US) in B mode and PD was performed at Achilles tendon (AT) and plantar fascia (PF). Results: The mean age of SpA patients was 41.9 ± 14.3 years and disease duration 8.4 ± 5.8 years. Axial form was found in 36 cases (90%) and peripheral form in 4 (10%). The mean ESR was 28.3 ± 23.2 mm/1sth and the CRP was 22.9 ± 31.2 mg/l. In SpA patients 109/160 (68.1%) of the assessed entheseal sites were significantly abnormal compared to 27/80 (33.8%) in M-LBP patients (AT p < .0001 and PF p = .02). Compared to the MLBP patients, a significant difference was found in AT for hypoechogenicity (p = .006) and bone erosion (p = .005) and at both entheses for cortical hypervascularisation (AT: p < .0001 and PF: p = .03). Otherwise, in SpA patients, 60.2% (53/88) of non tender entheses showed at least one ultrasound abnormality compared to 77.8% (56/72) of tender entheses. A significant correlation was identified between clinical and ultrasound assessment (r = 0.4, p = .01). Conclusion: The frequency of enthesitis was high among SpA compared with M-LBP patients and AT was the most affected enthesis. Abnormal vascularization in the cortical bone insertion of entheses was detected especially in SpA patients, and there was great evidence of subclinical enthesitis.

1. Introduction Enthesis is defined as a site of insertion of ligaments, joint capsule and tendons into bone. The term ‘‘enthesitis’’ is restricted to inflammation involving the entheses. Peripheral enthesitis, especially of lower limbs, has been repeatedly described as a hallmark in Spondyloarthritis (SpA). It distinguishes SpA from other inflammatory rheumatic disorders while the involvement of the entheses in any pathologic process, whether metabolic, inflammatory, traumatic, or degenerative, is referred to as enthesopathy [1]. In SpA, the frequency of peripheral enthesitis has been found to be within 25–58% [2], and in only 9.4% of cases according to the study of Abdelsalam et al. [3] but the real prevalence of this feature depends on the type of assessment (clinical, imaging or histological). Besides SpA patients, enthesitis is also frequent among athletes as a consequence of

traumatic injuries. Clinically, active enthesitis is defined as localised pain, tenderness and swelling at the site of an enthesis. However, there are no definite clinical criteria to diagnose these manifestations, which may even be asymptomatic and detected only by imaging, such as conventional radiography, bone scintigraphy, magnetic resonance imaging (MRI), or ultrasonography (US) [2–4]. Musculoskeletal ultrasonography (MSKUS) has proved to be a sensitive and non-invasive tool to assess the presence of enthesitis [4–14] which is characterised by tendon thickening, loss of tendon fibrillar pattern with hypoechogenicity, local calcifications, bony erosions and enthesophytes detected using B mode [11,12,14,15]. For more than a decade, several studies have shown the interest of ultrasound to detect enthesopathies, but considering that enthesitis of SpA is often underestimated or attributed by mistake to another cause, power Doppler US (PDUS) technology has allowed recently, the visualization of abnormal

Peer review under responsibility of Egyptian Society of Rheumatic Diseases. ⁎ Corresponding author at: Rheumatology Department, Farhat Hached Hospital, Faculty of Medicine, Sousse University, Ibn El Jazzar, Sousse, Tunisia. E-mail address: [email protected] (K. Baccouche). https://doi.org/10.1016/j.ejr.2017.11.002 Received 13 November 2017; Accepted 16 November 2017 1110-1164/ © 2017 Egyptian Society of Rheumatic Diseases. Publishing services provided by Elsevier B.V. All rights reserved. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/BY-NC-ND/4.0/).

Please cite this article as: Baccouche, K., The Egyptian Rheumatologist (2017), https://doi.org/10.1016/j.ejr.2017.11.002

The Egyptian Rheumatologist xxx (xxxx) xxx–xxx

K. Baccouche et al.

vascularisation at the insertion of the entheses into the cortical bone, which it is described as the typical sign of US enthesitis in SpA [13,14,16–18]. The aim of the present study was to assess the frequency and severity of peripheral enthesitis in SpA patients using US in B mode associated with power Doppler compared to a group of patients with mechanical low back pain (M-LBP).

Table 1 Demographic and clinical characteristics of the spondyloarthritis and mechanical low back pain patients.

2. Patients and methods Forty patients with established SpA were consecutively included in the study; they were 30 with ankylosing spondylitis (AS), 8 with psoriatic arthritis (PsA) and 2 with enteropathic arthritis (Crohn’s disease) and were meeting the Amor and New York modified criteria [19] and the CASPAR criteria for PsA [20]. 20 patients with M-LBP were included as a control group. Patients with another inflammatory or metabolic disease, chronic infection or cancer, lower limb trauma or surgery, having corticosteroid infiltration in the sites studied 6 weeks before or lower limb neuropathy were excluded. The study was approved by the appropriate medical ethic committee and patients gave informed consent before the start of the study. For all subjects both Achilles tendon (AT) and plantar fascia (PF) insertions on the calcaneus were examined by an experienced rheumatologist, unaware of the US results and recorded spontaneous pain, tenderness, mobilization of the corresponding tendons, and local swelling of the enthesis defining the presence of active clinical enthesitis. Medications received including non-steroidal anti-inflammatory drugs (NSAIDs), corticosteroids, disease-modifying antirheumatic drugs (DMARDs) and anti-TNF agents were recorded. Bath AS Disease Activity Index (BASDAI) and Functional Index (BASFI) were calculated [21,22]. C-reactive protein (CRP) and erythrocyte sedimentation rate (ESR) were considered. Musculoskeletal ultrasound (MSKUS) was performed on the same day of clinical assessment by a trained ultrasonographer blinded of the clinical examination findings using a Philips IU 22 machine with a 7.5MHz linear array transducer. Pulse repetition frequency was adjusted to the lowest permissible value to maximize sensitivity. The patient was lying prone and the feet were scanned in both longitudinal and transverse planes in B mode to detect morphologic abnormalities (thickness, bony erosion, enthesophyte and bursitis) and subsequently PDUS was performed to detect abnormal vascularisation. According to the Outcome Measures in Rheumatoid Arthritis Clinical Trials (OMERACT) Ultrasound consensus [23], bone erosion was defined as a discontinuity of the entheseal bone surface and enthesophyte as a hyperechoic prominence at the end of the entheseal bone contour seen in 2 perpendicular planes. Tendon thickness was measured at the point of maximal thickness proximal to the bony insertion. Vascularisation was studied at the cortical bone insertion using PDUS mode. US enthesitis was classified into 5 distinctive patterns according to the different combinations of abnormal gray-scale and/or PDUS features [24]. Statistical analysis: Statistical analysis was performed using the Statistical Package for Social Sciences software (SPSS 18.0, Chicago, IL). Quantitative variables were presented as mean ± SD and range. Differences between groups were tested by Chi-square test (categorical data) or Student’s unpaired t-test (numerical data). Pearson’s correlation test was considered. P values < .05 were considered significant.

Characteristic mean ± SD/n(%)

SpA patients (n = 40)

M-LBP patients (n = 20)

Sex male:female Age (years) Disease duration (years)

28:12 41.9 ± 14.3 8.4 ± 5.8

4:16 51.1 ± 11.5 3.5 ± 2.6

SpA subtype: AS PsA EA (Crohn’s disease)

30 (75) 8 (5) 2 (20)

NA

Tender enthesis BASDAI BASFI

19 (47.5) 5.1 ± 1.8 5.4 ± 2.4

7 (35) NA NA

Current treatment NSAIDs Anti-TNF-α

36 (90) 10 (25)

9 (45) NA

SpA: spondyloarthritis, M-LBP: mechanical low back pain, AS = ankylosing spondylitis; PsA = psoriatic arthritis; EA = enteropathic arthritis; BASDAI = Bath Ankylosing Spondylitis Disease Activity Index; NSAIDs = non steroidal antiinflammatory drugs; antiTNF = anti–tumor necrosis factor-α.

(17.5%) had previous uveitis. Axial form was found in 36 cases (90%) and peripheral form in 4 (10%). The mean ESR was 28.3 ± 23.2 mm/ 1st h and the CRP was 22.9 ± 31.2 mg/l. NSAIDs were used in 22 cases, corticosteroids in 9, sulfasalazine in 6, methotrexate in 11 and TNFα inhibitors in 10. In the 40 SpA patients by gray-scale combined with PDUS 109/160 (68.1%) of the entheseal sites (AT and PF) were significantly abnormal compared with 27/80 (33.8%) in patients with M-LBP (p < .0001 and p = .02 respectively), without significant variation in the frequency of US enthesitis among the different SpA subtypes (Table 2). In SpA patients, 47 of the 109 abnormal entheses (43.1%) presented abnormal vascularization in the cortical bone insertion; more found in the AT 34 (21.3%) compared with PF 13(8.1%) (Fig. 1a). In M-LBP patients, only 4 (5%) AT had a positive PD signal which was significantly lower than in the SpA patients (p < .0001). In axial SpA patients, decreased echogenicity is presented in Fig. 1b, bony erosion in Fig. 1c and enthesophyte in Fig. 1d. The distribution of enthesis involvement according to the 5 distinctive patterns is shown in Table 3. In M-LBP patients, the majority of entheseal abnormalities (23/27) were detected only in B mode and corresponded to stage 3b (22/27) with only 4/27 cases of vascularization on PDUS. Among the 40 SpA patients, 72/160 (45%) entheseal sites were tender and 77.8% of these patients had MSKUS abnormalities while 60.2% of patients without clinical enthesitis (n = 88) had subclinical abnormalities (Table 4). There were no gender differences. Of all entheses examined, 43.5% had imaging findings consistent with clinical examination. A significant correlation was identified between clinical and ultrasound assessment (r = 0.4, p = .01). No significant correlation was found between US findings and BASDAI, BASFI, treatment with NSAIDs or any second-line drugs (r = 0.06, r = 0.03, r = 0.009, r = 0.05, respectively).

4. Discussion

3. Results

All experts agree that peripheral enthesitis is a hallmark of SpA [13,14]. However, peripheral enthesitis is most certainly under-diagnosed during the course of SpA and the real prevalence of this feature depends on the type of assessment (clinical, imaging or histological). To our knowledge, there are no definite clinical criteria to diagnose these manifestations, which may even be asymptomatic and detected only by imaging such as US. In this study of an assessment of distal lower limbs entheses by US

The 40 patients with SpA (28 male, 12 female) had a mean age of and disease duration of 41.9 ± 14.3 years (22–83 years) 8.4 ± 5.8 years. The 20 M-LBP patients (4 male, 16 female) mean age was 51.1 ± 11.5 years (32–73 years) and disease duration of 3.5 ± 2.6 years. Demographic and clinical characteristics are shown in Table 1. In SpA patients, 3 (7.5%) had a family history of SpA and 7 2

The Egyptian Rheumatologist xxx (xxxx) xxx–xxx

K. Baccouche et al.

Table 2 Ultrasonographic findings of the Achillis tendon and plantar fascia in spondyloarthritis and mechanical low back pain patients. US abnormalities n (%)

Hypoechogenicity Tendon thickened Enthesophyte Bone erosion Positive PDUS

SpA patients (n = 40; 160 enthesis)

M-LBP patients (n = 20; 80 enthesis)

p

Total

AT

PF

Total

AT

PF

32 14 54 84 47

29 (18.1) 9 (5.6) 42 (26.3) 56 (35) 34 (21.3)

3 (1.9) 5 (3.1) 12 (7.5) 28 (17.5) 13 (8.1)

2 (2.5) 5 (6.3) 17 (21.3) 20 (25) 4 (5)

2 (2.5) 2 (2.5) 16 (20) 12 (15) 4 (5)

0 3 1 8 0

(20) (8.7) (33.8) (52.5) (29.4)

(0) (3.8) (1.3) (10) (0)

.006 .56 .44 .005 < .0001

n = number, SpA: spondyloarthritis, M-LBP: mechanical low back pain, AT: Achillis tendon, PF: plantar fascia, PDUS: power Doppler ultrasound.

assessed and by more severe disease observed in their study. Several authors have shown that positive PDUS signal especially in the cortical bone insertion is important because it enables distinction between inflammatory enthesitis, a hallmark of SpA and enthesitic lesions of mechanical origin [11,13,18,24]; this is consistent with our findings, as a significant difference was found between the two groups especially for PD vascularization. It has been shown that US assessment of inflammation at entheseal insertions could be dramatically improved by combining PDUS with B mode, resulting in the visualization of a pattern highly specific for SpA [24]. The performance of PDUS in detecting low-velocity blood flow at the microvascular level in several tissues has been demonstrated [25]. However, it is also well established that the performance of PDUS can be influenced by the examiner, the machine, and the acoustical conditions involved in image processing [26]. In our current work, ultrasound showed to be a sensitive tool in detecting enthesitis and subclinical enthesitis that can be missed during routine clinical examination, thus, it is largely confirmed that US examination was more sensitive than clinical examination for tenderness; these data were previously reported by others [11,13,18,25,27,28]. The

examination in B mode and PDUS in SpA patients compared to patients with mechanical LBP, there were several findings. First, the frequency of enthesitis was higher among SpA patients and AT was the most affected enthesis. Second, there was no significant variation in the frequency of US enthesitis among the different subtypes of SpA which is consistent with the concept that they represent phenotypic variations of a unique disease. Third, abnormal vascularization in the cortical bone insertion (positive PDUS signals) of affected entheses was detected especially in SpA patients. Finally, there was a trend toward a more severe pattern of US involvement among SpA patients with evidence of subclinical enthesitis. The percentage of ultrasound enthesitis was higher in SpA patients. Bony erosion was frequent as one of the known abnormalities in established SpA, but bony spurs were frequent in both patients groups, highlighting the difficulty in differentiating mechanical spurs from true enthesophytes. Abnormal vascularization in the cortical bone insertion was significantly higher in SpA patients. However, in the study of D’Agostino et al. [24], 98% of the SpA patients had at least one vascularized enthesitic site. This difference could be explained by the higher number of entheses

Fig. 1. Musculoskeletal ultrasonographic findings on the Achillis tendon (AT) in patients with axial spondyloarthritis: (a) Left AT of 28-year-old man showing abnormal vascularization in the cortical bone insertion (positive power Doppler signals), (b) Left AT of a 40 years old woman showing decreased echogenicity (arrow), (c) Right AT in a 45-years old man showing erosion and positive power Doppler signals in the cortical bone insertion and in erosion (d) Left AT in a 30 year old man showing enthesophyte (arrow).

3

The Egyptian Rheumatologist xxx (xxxx) xxx–xxx

K. Baccouche et al.

Table 3 Classification of abnormal peripheral enthesis by musculoskeletal ultrasound in spondyloarthritis and mechanical low back pain patients. US staging n (%)

SpA patients (n = 40; 160 enthesis)

Abnormality Positive PDUS Stage 1 Stage 2a Stage 3a Negative PDUS Stage 2b Stage 3b

M-LBP patients (n = 20; 80 enthesis)

Total

AT

PF

Total

AT

PF

51 (31.9) 47 (29.4) 7 (4.5) 1 (0.6) 39 (24.4) 62 (38.8) 2 (1.3) 60 (37.5)

12 (7.5) 34 (21.3) 4 (2.5) 1 (0.6) 29 (18.1) 34 (21.3) 0 (0) 34 (21.25)

39 (24.4) 13 (8.1) 3 (2) 0 (0) 10 (6.3) 28 (17.5) 2 (1.3) 26 (16.25)

53 (66.3) 4 (5) 0 (0) 0 (0) 4 (5) 23 (28.8) 1 (1.25) 22 (27.5)

22 (27.5) 4 (5) 0 (0) 0 (0) 4 (5) 14 (17.5) 0 (0) 14 (17.5)

31 (38.8) 0 (0) 0 (0) 0 (0) 0 (0) 9 (11.3) 1 (1.3) 8 (10)

SpA: spondyloarthritis, M-LBP: mechanical low back pain, AT: Achillis tendon, PF: plantar fascia, PDUS: power Doppler ultrasound.

Conflict of interest

Table 4 Musculoskeletal ultrasound assessment in spondyloarthritis patients with and without clinical enthesitis.

None.

Spondyloarthritis patients (n = 40; 160 enthesis)

Funding Clinical enthesitis

Hypoechogenicity Tendon thickened Enthesophyte Bone erosion Positive PDUS

Total

with (n = 72)

without (n = 88)

p

32 14 54 84 47

18 10 31 44 24

14 (8.75) 4 (2.5) 23 (14.4) 40 (25) 23 (14.4)

0.73 0.27 0.67 1 0.84

(20) (8.8) (33.8) (52.5) (29.4)

(11.25) (6.3) (19.4) (27.5) (15)

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. References [1] Khan MA. Update on spondyloarthropathies. Ann Intern Med 2002;136:896–907. [2] Olivieri I, Barozzi L, Padula A. Enthesiopathy: clinical manifestations, imaging and treatment. Baillieres Clin Rheumatol 1998;12:665–81. [3] Abdelsalam A, Tharwat S, AboAlmauty M, Barakat AF, Enein AF, Abdelsalam N, et al. Demographic, clinical and radiological characteristics of seronegative spondyloarthritis Egyptian patients: a rheumatology clinic experience in Mansoura. Egypt Rheumatol 2017;39(2):109–14. [4] Gandjbakhch F, Terslev L, Joshua F, Wakefield RJ, Naredo E, D'Agostino MA, et al. Ultrasound in the evaluation of enthesitis: status and perspectives. Arthritis Res Ther 2011;13:R188. [5] Hassan AA, Darwish AF, Mohamed FA, Ibrahim MA, Abd El-Karim AH. Value of musculoskeletal ultrasonography in the diagnosis of peripheral enthesopathy in early spondyloarthropathy. Egypt Rheumatol Rehabil 2014;41:51–7. [6] D’Agostino MA. Ultrasound imaging in spondyloarthropathies. Best Pract Res Clin Rheumatol 2010;24:693–700. [7] Falsetti P, Frediani B, Fioravanti A, Acciai C, Baldi F, Filippou G, et al. Sonographic study of calcaneal entheses in erosive osteoarthritis, nodal osteoarthritis, rheumatoid arthritis and psoriatic arthritis. Scand J Rheumatol 2003;32:229–34. [8] Filippucci E, Aydin SZ, Karadag O, Salaffi F, Gutierrez M, Direskeneli H, et al. Reliability of high-resolution ultrasonography in the assessment of Achilles tendon enthesopathy in seronegative spondyloarthropathies. Ann Rheum Dis 2009;68:1850–5. [9] Aydin SZ, Karadag O, Filippucci E, Atagunduz P, Akdogan A, Kalyoncu U, et al. Monitoring Achilles enthesitis in ankylosing spondylitis during TNF-alpha antagonist therapy: an ultrasound study. Rheumatology (Oxford) 2010;49:578–82. [10] Naredo E, Batlle-Gualda E, García-Vivar ML, García-Aparicio AM, Fernández-Sueiro JL, Fernández-Prada M, et al. Power Doppler ultrasonography assessment of entheses in spondyloarthropathies: response to therapy of entheseal abnormalities. J Rheumatol 2010;37:2110–7. [11] Zhang H, Liang J, Qiu J, Wang F, Sun L. Ultrasonographic evaluation of enthesitis in patients with ankylosing spondylitis. J Biomed Res 2017;31:162–9. [12] Sudoł-Szopińska I, Zaniewicz-Kaniewska K, Saied F, Kunisz W, Smorawińska P, Włodkowska-Korytkowska M. The role of ultrasonography in the diagnosis of rheumatoid arthritis and peripheral spondyloarthropathies. Pol J Radiol 2014;79:59–63. [13] Sakellariou G, Iagnocco A, Delle Sedie A, Riente L, Filippucci E, Montecucco C. Ultrasonographic evaluation of entheses in patients with spondyloarthritis: a systematic literature review. Clin Exp Rheumatol 2014;32:969–78. [14] Terslev L, Naredo E, Iagnocco A, Balint PV, Wakefield RJ, Aegerter P, et al. Defining enthesitis in spondyloarthritis by ultrasound: results of a Delphi process and of a reliability reading exercise. Arthritis Care Res (Hoboken) 2014;66:741–8. [15] Yang J, Zhang H, Zhou B, Zhu J, Zhang J, Huang F. The distinctive characteristics of ultrasonic imaging of enthesitis in spondyloarthritis patients. Zhonghua Nei Ke Za Zhi 2015;54:628–32. [16] Balint PV, Kane D, Wilson H, McInnes IB, Sturrock RD. Ultrasonography of entheseal insertions in the lower limb in spondyloarthropathy. Ann Rheum Dis 2002;61:905–10. [17] Grassi W, Salaffi F, Filippucci E. Ultrasound in rheumatology. Best Pract Res Clin Rheumatol 2005;19:467–85. [18] Freeston JE, Coates LC, Helliwell PS, Hensor EM, Wakefield RJ, Emery P, et al. Is there subclinical enthesitis in early psoriatic arthritis? A clinical comparison with

PDUS: power Doppler ultrasound.

high number of subclinical enthesitis was found especially in AT which has also been reported [24]. In a study on Egyptian SpA patients enthesis involvement was found to occur early and the enthesis US score appeared to be reliable and useful for improving the diagnostic accuracy [29]. These data suggest that enthesitis, which could partly result from biomechanical stress forces, may happen where such forces predominate (distal entheseal sites of the lower limbs), both in inflammatory and mechanical diseases. Furthermore, such events might be amplified in the context of SpA [11,24]. The entheses US score adopted by D’Agostino et al. [24] used in our study also trended toward a more severe pattern of US involvement among SpA patients. This tool appears to be valid and may be useful for improving the follow up and the diagnostic accuracy of early SpA and is in accordance with the results of Balint et al. [16] who showed that US GUESS (Glasgow Ultrasound Enthesitis Scoring System) score is superior in detecting entheseal abnormalities in the lower limbs of SpA and with Alcalde et al. [30] who showed that a scoring method such as the SEI (Sonographic Enthesis Index) may be of help in characterizing entheseal injury in AS, moreover, de Miguel et al. who concluded that MASEI (Madrid Sonographic Enthesis) ultrasound enthesis score could be a valid tool in the diagnosis of SpA [25]. The study had some limitations; for feasibility reasons, only AT and PF entheses were assessed by ultrasound. This exclusion of number of entheses may reduce the ability to draw conclusions regarding the frequency of enthesitis but it was widely demonstrated that these two entheses were the most frequently abnormal sites in SpA [13,16] and our results agree with those of the literature. Furthermore, the assessment of tendons by US was performed in a neutral but not relaxed position, which can reduce the sensitivity and signal of PD [26]. In summary, ultrasonography can be useful for detecting subclinical enthesitis in SpA patient and the enthesis US score can be useful for improving the diagnostic and monitoring of SpA. However, to evaluate and validate the diagnostic and follow-up value of US, longitudinal multicenter studies with early disease and still-uncertain diagnoses patients are still needed. 4

The Egyptian Rheumatologist xxx (xxxx) xxx–xxx

K. Baccouche et al.

Rheum 2003;48:523–33. [25] de Miguel E, Munoz-Fernandez S, Castillo C, Cobo-Ibáñez T, Martín-Mola E. Diagnostic accuracy of enthesis ultrasound in the diagnosis of early spondyloarthritis. Ann Rheum Dis 2011;70:434–9. [26] Gutierrez M, Filippucci E, Grassi W, Rosemffet M. Intratendinous power Doppler changes related to patient position in seronegative spondyloarthritis. J Rheumatol 2010;37:1057–9. [27] Michelsen B, Diamantopoulos AP, Soldal DM, Hammer HB, Kavanaugh A, Haugeberg G. Achilles enthesitis defined by ultrasound is not associated with clinical enthesitis in patients with psoriatic arthritis. RMD Open 2017;3:e000486. [28] Galluzzo E, Lischi DM, Taglione E, Lombardini F, Pasero G, Perri G, et al. Sonographic analysis of the ankle in patients with psoriatic arthritis. Scand J Rheumatol 2000;29:52–5. [29] Ezzat Y, Gaber W, Abd EL-Rahman SF, Ezzat M, El Sayed M. Ultrasonographic evaluation of lower limb enthesis in patients with early spondyloarthropathies. Egypt Rheumatol 2013;35(1):29–35. [30] Alcalde M, Acebes JC, Cruz M, González-Hombrado L, Herrero-Beaumont G, Sánchez-Pernaute O. A sonographic enthesitic index of lower limbs is a valuable tool in the assessment of ankylosing spondylitis. Ann Rheum Dis 2007;66:1015–9.

power doppler ultrasound. Arthritis Care Res 2012;64:1617–31. [19] Van der Linden SM, Valkenburg HA, Cats A. Evaluation of the diagnosis criteria for ankylosingsponlylitis: a proposal for modification of the New York criteria. Arthritis Rheum 1984;27:361–8. [20] Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H, et al. Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum 2006;54:2665–73. [21] Calin A, Garrett S, Whitelock H, Kennedy LG, O'Hea J, Mallorie P, et al. A new approach to defining functional ability in ankylosing spondylitis: the development of the Bath Ankylosing Spondylitis Functional Index. J Rheumatol 1994;21:2281–5. [22] Garrett S, Jenkinson T, Kennedy LT, Whitelock H, Gaisford P, Calin A. A new approach to defining diseases status in ankylosing spondylitis: the Bath Ankylosing Spondylitis Disease Activity Index. J Rheumatol 1994;21:2286–91. [23] Wakefield RJ, Balint PV, Szkudlarek M, Filippucci E, Backhaus M, D'Agostino MA, et al. Musculoskeletal ultrasound including definitions for ultrasonographic pathology. J Rheumatol 2005;32:2485–7. [24] D’Agostino MA, Said-Nahal R, Hacquard-Bouder C, Brasseur JL, Dougados M, Breban M. Assessment of peripheral enthesitis in the spondyloarthropathies by ultrasonography combined with power Doppler: a cross-sectional study. Arthritis

5