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 Table of Contents  
ORIGINAL ARTICLE
Year : 2017  |  Volume : 12  |  Issue : 4  |  Page : 199-203

Evaluation of peripheral enthesitis in spondyloarthritis: Ultrasonography versus clinical examination


Department of Rheumatology, KGMU, Lucknow, Uttar Pradesh, India

Date of Web Publication16-Nov-2017

Correspondence Address:
Saumya Ranjan Tripathy
Department of Rheumatology, KGMU, Lucknow - 226 001, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/injr.injr_39_17

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  Abstract 


Background: Enthesitis is an important feature of spondyloarthritis but may often be subclinical. Data is sparse, especially from India, on the ultrasonography (USG) detection of enthesitis in these patients. The present study aimed to find the prevalence and pattern of entheseal involvement assessed clinically and by USG.
Methods: Fifty-two spondyloarthritis, 26 rheumatoid arthritis, and 26 healthy controls were evaluated for enthesitis by clinical examination and by USG using 2014 OMERACT consensus group definitions at bilateral Achilles insertion on the calcaneus, plantar fascia attachment on the calcaneus, quadriceps tendon insertion on the patella, patellar tendon origin from the inferior pole of the patella, and patellar tendon insertion on the tibial tuberosity. At least one ultrasonographic finding at any of the above sites was considered positive for enthesitis.
Results: The number of entheseal sites screened in spondyloarthritis patients was 520 and 260 each in rheumatoid arthritis and healthy controls. USG (sensitivity - 94.2%) was better in detecting enthesitis than clinical examination (sensitivity - 69.2%). Clinical examination was highly specific (100%) compared to USG (55.7%) in differentiating from rheumatoid arthritis and healthy controls. USG alone without clinical findings was positive at 23.8% of sites while clinical examination alone without USG findings was positive at 5.2% of sites. Frequency of enthesitis in rheumatoid arthritis was not more than healthy controls (6.1% vs. 8.1%, respectively) and was much less than spondyloarthritis (34%).
Conclusion: USG is a good screening tool for detection of enthesitis but cannot replace clinical examination completely.

Keywords: Enthesitis, spondyloarthritis, ultrasonography


How to cite this article:
Wakhlu A, Tripathy SR, Wakhlu A, Srivastava D, Sahoo RR. Evaluation of peripheral enthesitis in spondyloarthritis: Ultrasonography versus clinical examination. Indian J Rheumatol 2017;12:199-203

How to cite this URL:
Wakhlu A, Tripathy SR, Wakhlu A, Srivastava D, Sahoo RR. Evaluation of peripheral enthesitis in spondyloarthritis: Ultrasonography versus clinical examination. Indian J Rheumatol [serial online] 2017 [cited 2019 Oct 22];12:199-203. Available from: http://www.indianjrheumatol.com/text.asp?2017/12/4/199/211695




  Introduction Top


Spondyloarthritis is a group of disorders sharing common features such as inflammatory back pain, asymmetric large joint predominant arthritis and negative rheumatoid factor.[1] Enthesitis is an important clinical feature shared by the different spondyloarthritis. It is defined as the inflammation of insertion sites of tendons, ligaments, fascia, and joint capsules on the bony surface.[2] Enthesitis can often be subclinical. Ultrasonography (USG) is an upcoming modality of investigation for enthesitis. In 2014, the OMERACT consensus group released a statement regarding USG evaluation of enthesitis.[2]

There are limited data, especially from India regarding ultrasonographic evaluation of enthesitis in spondyloarthritis. The available data predate the release of the OMERACT consensus group definitions of enthesitis. Thus, it is necessary to re-evaluate enthesitis in spondyloarthritis using USG keeping the above definitions in mind. The primary objective of our study was to find the prevalence and pattern of entheseal site involvement as assessed clinically and by USG.


  Methods Top


Fifty-two patients with spondyloarthritis (satisfying either Assessment of SpondyloArthritis International Society [ASAS] classification criteria for axial spondyloarthropathy or ASAS classification criteria for peripheral spondyloarthropathy) between 16 and 55 years age, presenting to the department of rheumatology at a tertiary care hospital, were included in the study. Age- and sex-matched 26 patients with rheumatoid arthritis and 26 healthy participants were selected as controls. Healthy individuals were defined as individuals without any musculoskeletal complaints or extra-articular manifestations of spondyloarthritis and without any family history ( first-degree blood relatives) of inflammatory arthritis. Any participant who had a prior history of trauma or surgery of the knees or ankles, diabetes mellitus, peripheral neuropathy of the lower limbs, or corticosteroid injections at entheseal sites under evaluation were excluded from the study.

The entheseal sites included for evaluation were (1) insertion of quadriceps at the superior pole of patella, (2) origin of patellar tendon from the inferior pole of patella, (3) insertion of patellar tendon at tibial tuberosity, (4) Achilles tendon (AT) insertion on the calcaneus, and (5) plantar fascia (PF) attachment on the calcaneus.

The entheseal sites were examined clinically by applying digital pressure enough to partially blanch the nail of the thumb at the local site and evaluation for the presence or absence of tenderness. USG evaluation was done using multifrequency linear array transducer (8–13 MHz) of Logiq E; GE Medical System's ultrasound machine. For gray scale (GS) images, the B-mode settings were kept as dynamic range (40–50 dB), GS frequency (10–13 MHz), and GS gain (50–80 dB). For power Doppler (PD) images, the settings used were pulsed repetition frequency (400–800 Hz) and PD gain (highest possible gain with minimum background noise).

For the USG examination, the patients were comfortably positioned on the examination couch, and probe placement was done as described by Naredo et al.[3] For screening quadriceps tendon (QT) on the superior pole of patella, patellar tendon origin (PTO) from the inferior pole of patella, and patellar tendon insertion (PTI) on the tibial tuberosity, the patient was positioned in supine decubitus while for AT insertion on the calcaneus and PF attachment on the calcaneus, the patient was placed in prone position with the feet hanging outside the examination table. For GS imaging, the knee was flexed 30° for QT and 45° for PTO and PTI, while for PD images at the above threes sites (QT, PTO, and PTI), the knee was placed in neutral position. For AT and PF, the foot was kept in slight dorsiflexion for GS imaging and in neutral position for PD. The probe was placed over the proximal pole of the patella for QT, distal pole of patella for PTO, anterior tibial tuberosity for PTI, posterior and superior aspect of the calcaneus for AT, and plantar aspect of the calcaneus for PF. For each site, both longitudinal and transverse planes were evaluated. Enthesitis was deemed to be present if any of the structural findings or PD signals as defined by the OMERACT consensus group was found to be present [Table 1].[2]
Table 1: Outcome Measures in Rheumatology Clinical Trials definitions of ultrasonography findings of enthesitis

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Ethical approval

This study was approved by the Ethics Committee of our institution. Informed written consent was obtained from all patients before their enrollment in this study.


  Results Top


The study was completed in 6 months. The participants in different groups were age and sex matched. The demographic data are shown in [Table 2].
Table 2: Demographic characteristics of patients

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Out of 52 spondyloarthritis patients, 37 patients had ankylosing spondylitis, 11 had psoriatic arthritis, and 2 patients each had reactive arthritis and inflammatory bowel disease-associated arthritis.

A total of 520 entheseal sites were screened for patients with spondyloarthritis, 260 entheseal sites each for rheumatoid arthritis, and healthy controls. [Figure 1] shows a representative image of USG findings of enthesitis. [Table 3] shows the distribution of enthesitis detected by USG and clinical examination.
Figure 1: Representative ultrasonography image of Achilles tendon insertion enthesitis (on the calcaneus) showing increased thickness (yellow bracket), erosion (white arrow), hypoechogenicity (yellow asterisk), and presence of grade 2 power Doppler signals (bright red spots)

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Table 3: Distribution of enthesitis (ultrasonography vs. clinical examination)

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Clinical examination detected enthesitis in patients with spondyloarthritis only, while enthesitis was detected by USG in all three groups [Table 3]. However, the frequency of USG-detected enthesitis in rheumatoid arthritis (6.1%) was similar to that in healthy controls (8.1%) and far less compared to spondyloarthritis (34%). USG alone without clinical findings was positive at 23.8% of sites while clinical examination alone without USG findings was positive at 5.2% of sites.

Assuming enthesitis to be present in all spondyloarthritis patients, clinical examination has a sensitivity of 69.2% and specificity of 100% while USG has a sensitivity and specificity of 94.2% and 55.7%, respectively.

Enthesitis by USG was most frequently detected at the insertion of AT followed by the PTO [Table 3].

The distribution of various USG features of enthesitis is shown in [Table 4]. Increased thickness, PD signals, and hypoechogenicity are more common findings in spondyloarthritis. In nonspondyloarthritis patients, the most common findings are increased thickness and enthesophytes while the prevalence of PD signals, erosions, hypoechogenicity, and intratendinous calcifications is low.
Table 4: Frequency of ultrasound findings

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In the spondyloarthritis group, increased thickness was the most common finding (17.7%) followed by PD signals (15.2%) and hypoechogenicity (12.5%) [Figure 1].


  Discussion Top


In this study we appraised the pattern and prevalence of enthesitis in light of the new OMERACT consensus group definition of enthesitis by USG and compare it to clinical detection. Overall, USG performed better than clinical examination in the detection of enthesitis, but detection by USG does not always correlate with clinical examination and vice versa. Clinical examination was found to be more specific and could pick up enthesitis in approximately 5% of patients who had no findings on USG. AT insertion was found to be the most common site of enthesitis and increased thickness to be the most common finding on USG.

The prevalence of enthesitis was found to be 69.2% among spondyloarthritis patients on clinical examination. This is higher compared to Western data (25%–28% for ankylosing spondylitis) but lower compared to another study by Ghatak and Shanmuganandan, from India, which had detected a prevalence of 88%.[4],[5] This could be due to the different sites include for the two studies. It was observed that USG (sensitivity 94.2%) performed better than clinical examination (sensitivity 69.2%) in detecting enthesitis. The sensitivity of USG detected in the current study is in line with the study by D'Agostino et al., which showed a sensitivity of 98% and MAdrid Sonographic Enthesitis Index (MASEI) score which had a sensitivity of 83.3%.[6],[7] It is higher than the pilot study done by Danda et al. from India which showed a sensitivity of 40%.[8] This could be because of technological advance in USG machine, more standardized definitions, and inclusion of PD signals in the definition of enthesitis.

However, there appeared to be discrepancy between USG and clinical findings. Although USG-detected enthesitis in 23.8% of entheseal sites which were clinically normal, 5.2% of sites with enthesitis on clinical examination did not reveal any USG finding including PD signals. This discrepancy was also reflected by the study by Kiris et al., in which three out of four patients who did not have tenderness on clinical examination had abnormality on USG, whereas three patients who had tenderness on clinical examination had no USG abnormality.[9] This suggests that both methods are necessary for the evaluation of enthesitis and USG cannot completely replace clinical examination.

On comparing clinical examination in patients with and without spondyloarthritis (rheumatoid arthritis and healthy controls), it was observed that clinical examination was highly specific (100%) while it had low sensitivity (69.2%). On the other hand, USG had a high sensitivity (94.2%) but low specificity (55.7%). This implies that USG can be a good screening tool and can be used to detect enthesitis where the diagnosis of spondyloarthritis is elusive or in doubt while clinical examination is used for diagnosis of spondyloarthritis-specific enthesitis. An important caveat to this finding is that the study included only rheumatoid arthritis and healthy controls where enthesitis is expected to be absent. There are other causes of enthesitis, for example, crystal arthropathy (calcium pyrophosphate and uric acid), age-related degenerative changes, trauma, diffuse idiopathic skeletal hyperostosis, fluoride intoxication, chronic retinoid toxicity, and endocrine disorders such as acromegaly.[8] Studies must be conducted to find sensitivity and specificity of clinical examination and USG in differentiating enthesitis due to spondyloarthritis from nonspondyloarthritis causes.

The definition of enthesitis detected by USG was the presence of at least one USG finding at any entheseal site screened. This is the most probable cause for low specificity. The use of an USG score, with differential weightage to different parameters, may increase the specificity of USG. This is suggested by the recently developed BUSES score where the presence of erosions and PD score was scored higher than other parameters.[10] The BUSES score had a specificity of 90.7% but sensitivity was 47%, which makes it a suboptimal screening measure. Many scores have been described including GUESS, D'Agostino's score, MASEI, and sonographic enthesitis index.[11] However, these were before the OMERACT consensus definitions. Hence, there is a need for studies with larger number of participants for the development of a new score which balances sensitivity and specificity and makes USG more relevant.

Our study had several limitations. First, the small sample size in this study may not reflect the exact clinical and USG prevalence and pattern of enthesitis in spondyloarthritis. Second, one needs to evaluate the performance of USG vis-a-vis clinical examination in cases of enthesitis other than spondyloarthritis and rheumatoid arthritis. Third, hospital-based recruitment at a tertiary care center where more severe patients turn up increases the chance of inclusion of clinically apparent enthesitis.

In conclusion, our study found that USG had high sensitivity and moderate specificity compared to clinical examination in the detection of enthesitis. Clinical examination has a high specificity in differentiating enthesitis in spondyloarthritis from rheumatoid arthritis and healthy individuals. PD signals, hypoechogenicity, and erosions are more commonly seen in spondyloarthritis-related arthritis. Ultrasound has the potential to be used as a screening tool for enthesitis and research is required for the development of an USG score with high sensitivity and specificity to enable its widespread usage.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Hochberg MC, Silman AJ, Smolen JS, Weinblatt ME, Weismann MH, editors. Classification and epidemiology of spondyloarthritis. In: Rheumatology. 6th ed., Ch. 113. Philadelphia: Elsevier Mosby; c2015. p. 941-5.  Back to cited text no. 1
    
2.
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.  Back to cited text no. 2
    
3.
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.  Back to cited text no. 3
    
4.
Hochberg MC, Silman AJ, Smolen JS, Weinblatt ME, Weismann MH, editors. Enthesopathies. In: Rheumatology. 6th ed., Ch. 123. Philadelphia: Elsevier Mosby; c2015. p. 1014-20.  Back to cited text no. 4
    
5.
Ghatak S, Shanmuganandan K. A study of enthesitis in spondyloarthropathy in patients from tertiary care service hospital. J Evol Med Dent Sci 2014;3:7822-30.  Back to cited text no. 5
    
6.
D'Agostino MA, Said-Nahal R, Hacquard-Bouder C, Brasseur JL, Dougados M, Breban M. Assessment of peripheral enthesitis in the spondylarthropathies by ultrasonography combined with power Doppler: A cross-sectional study. Arthritis Rheum 2003;48:523-33.  Back to cited text no. 6
    
7.
de Miguel E, Cobo T, Muñoz-Fernández S, Naredo E, Usón J, Acebes JC, et al. Validity of enthesis ultrasound assessment in spondyloarthropathy. Ann Rheum Dis 2009;68:169-74.  Back to cited text no. 7
    
8.
Danda D, Shyam Kumar NK, Cherian R, Cherian AM. Enthesopathy: Clinical recognition and significance. Natl Med J India 2001;14:90-2.  Back to cited text no. 8
    
9.
Kiris A, Kaya A, Ozgocmen S, Kocakoc E. Assessment of enthesitis in ankylosing spondylitis by power Doppler ultrasonography. Skeletal Radiol 2006;35:522-8.  Back to cited text no. 9
    
10.
Milutinovic S, Radunovic G, Veljkovic K, Zlatanovic M, Zlatkovic Svenda M, Perovic Radak M, et al. Development of ultrasound enthesitis score to identify patients with enthesitis having spondyloarthritis: Prospective, double-blinded, controlled study. Clin Exp Rheumatol 2015;33:812-7.  Back to cited text no. 10
    
11.
Mata Arnaiz MC, de Miguel Mendieta E. Usefulness of ultrasonography in the assessment of peripheral enthesis in spondyloarthritis. Reumatol Clin 2014;10:113-9.  Back to cited text no. 11
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]


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2 Ultrasonography in the evaluation of peripheral enthesitis in spondyloarthropathy
Sumeet Agrawal,Ashok Kumar
Indian Journal of Rheumatology. 2017; 12(4): 190
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