Ultrasound imaging for sternoclavicular joint involvement in enthesitis-related arthritis: A closer look at capsular enthesitis

Introduction

Juvenile idiopathic arthritis (JIA) is the most common rheumatic disease in children, defined by arthritis of unknown origin that begins before 16 years of age and persists for at least 6 weeks. ¹ Enthesitis-related arthritis (ERA) accounts for 10%–30% of JIA cases, and the diagnosis requires the co-presence of arthritis and enthesitis or the evidence of one of them coupled with at least two additional diagnostic criteria. Sacroiliac joint tenderness, inflammatory back pain, presence of human leukocyte antigen (HLA)-B27, acute symptomatic anterior uveitis, onset in a male child aged 6 years or older or history of spondyloarthropathy in a first-degree relative are the additional diagnostic criteria. ² ERA presents several clinical features similar to adult spondyloarthritis but, unlike adults with ankylosing spondylitis, children show greater peripheral joint involvement. ² Peripheral arthritis in ERA typically is asymmetric and often involves large joints of the lower limbs, like the knee, hip and ankle. ³ Small joints like the sternoclavicular joint (SCJ) are rarely affected, and the prevalence of their involvement in JIA, and ERA specifically, has been poorly assessed in the pertinent literature. ⁴ Ultrasound (US) can be considered a powerful diagnostic tool for several reasons in the paediatric population with JIA/ERA. A high-frequency linear transducer is required to obtain high-resolution imaging of structures with limited overlying soft tissues such as the SCJ. Moreover, a dynamic US examination to differentiate the intra-articular effusion from the immature skeleton’s abundant hypo/anechoic cartilage can be performed. Finally, the lack of ionising radiations allows the clinician to use US imaging as a useful diagnostic tool to monitor the patient during the follow-up phase and optimise the pharmacological treatment. Sulfasalazine is the therapy of choice for children with ERA and peripheral arthritis but, anti-tumour necrosis factor (TNF) represents the second-line treatment for those showing moderate-to-high disease activity despite first-line therapy. ⁵

The authors report an interesting case describing the pivotal role of point-of-care US in identifying the SCJ involvement in a 12-year-old boy with ERA due to poor control of activity disease with first-line pharmacological agents. In this sense, sonographic and physical examination should not be considered different steps of the diagnostic pathway but rather the two faces of the clinical assessment.

Case report

A 12-year-old male child has been referred to our Paediatric Emergency Department due to pain in the left gluteal region onset 1 month before, coupled with functional limitation in external rotation of the hip, limping and morning stiffness. His medical history was negative for trauma and fever; paracetamol had been poorly effective for pain management at home. At the emergency department, blood exams, hip US and pelvis X-ray showed no abnormalities; so, a 14-day pharmacological therapy with ibuprofen was prescribed and the patient was discharged.

Two weeks later, due to the failure of non–steroidal anti-inflammatory drugs (NSAID) therapy, magnetic resonance imaging (MRI) of the pelvis and left lower limb was performed showing bilateral sacroiliitis (Figure 1), left knee synovitis and enthesitis of the ipsilateral patellar tendon and plantar fascia. The patient was hospitalised in our Paediatric Department, and a US-guided intra-articular injection of the left knee (triamcinolone hexacetonide 40 mg) was coupled with naproxen (15 mg/kg/die) as a bridge therapy to go further with the diagnostic workup and exclude neoplastic disorders and infections.

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Figure 1.

MRI shows bilateral sacroiliitis (A, B) with bone marrow oedema (yellow arrowheads) and periarticular effusion (white arrowheads) spilling within the surrounding pelvic muscles on the left side (A, C).

Creatine kinase, ferritin, coagulation, quantiferon, urine analysis, uric acid, calcium-phosphorus metabolism, complements C3 and C4, antistreptolysin O titre (ASLOT), NSE, 24 h urine vanillylmandelic acid, homovanillic acid, faecal calprotectin, complete blood count (CBC), C-reactive protein (CRP), renal and hepatic function were normal. The ESR was elevated (62 mm/h; normal <30 mm/h). HLA typing resulted positive for B27. Autoimmunity markers showed a weak positivity of anti-nuclear antibody (ANA) with a title of 1:160 speckled pattern and absence of rheumatoid factor (RF), anti-citrullinated peptides (anti-CCP), anti-double-strand DNA (anti-dsDNA) and anti-extractable nuclear antigen (ENA). Electrocardiogram, heart US, chest X-ray and US abdominal were normal. No inflammatory signs in the anterior chamber of the eyes to the slit lamp examination were observed.

The age of onset of symptoms, the concurrent presence of arthritis (sacroiliac joint and knee) with enthesitis (patellar tendon and plantar fascia), HLA-B27 positive and exclusion of a wide range of differential diagnoses of limping have been considered highly suggestive of ERA. During hospitalisation due to the poor control of activity disease with persistence of the aforementioned clinical findings, naproxen was progressively replaced with sulfasalazine 40 mg/kg/die, an immunosuppressive agent commonly used in patients with moderately active ERA. Despite the step-up of pharmacological treatment from naproxen to sulfasalazine, the patient progressively developed left SCJ tenderness and swelling in the following 30 days.

So, a point-of-care US examination comparing the healthy and painful side was performed by clinicians. Indeed, especially in paediatric patients, a comparative US scanning is paramount to optimise the differentiation (often tricky) between physiological and pathological findings. A large amount of gel – that is, suspension technique – has been used to reduce unintentional compression of the superficial soft tissues with the transducer and avoid a squeeze of the articular effusion and small blood vessels. Hypertrophy of the synovial tissue, intra-articular effusion and capsular thickening of the left SCJ were the sonographic findings reported in B-mode (Figure 2). Moreover, comparative scanning showed a remarkable bulging of the superior and anterior surface of the joint capsule on the painful side compared to the normal one. Compressing the capsular bump local pain was evoked – that is, positive sono-compression. ⁶ An accurate colour Doppler (CD) setting by adjusting the size of the region of interest and the pulse repetition frequency depicted an intense hypervascularisation of the joint capsule, the synovial tissue and the capsule–bone junction (Figure 2). ⁶ Interestingly, aberrant vascular signals have been observed at the capsular enthesis on the clavicular side but not on the sternal one.

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Figure 2.

Comparative B-mode ultrasound of the sternoclavicular joint (A) showed articular effusion (white asterisk) coupled with capsular bulging (white dotted line) on the left side. Colour Doppler (CD) assessment (B, C) depicted hypervascularisation involving the joint capsule (white arrowhead), the synovial fringe (yellow arrowhead) and the capsule–bone interface (red arrowhead). Cl: clavicle, St: sternum, CD: colour Doppler.

The persistence of left gluteal pain and limping coupled with the onset of left SCJ arthritis/enthesitis has been considered a progression of the ERA due to poor control of the activity disease using the sulfasalazine 40 mg/kg/die (Table 1). In this sense, the pharmacological treatment was progressively modified by increasing sulfasalazine to 50 mg/kg/die and introducing a biological disease-modifying anti-rheumatic drug–adalimumab 40 mg (subcutaneous injection) every 2 weeks. Before starting the adalimumab, a whole-body MRI confirmed the left SCJ inflammatory changes and showed bone marrow oedema on the clavicular and sternal side of the joint (Figure 3).

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Table 1.

From diagnosis to treatment: a step-by-step approach.

Diagnostic pathway	Pharmacological treatment	Timeline
Clinical onset (left gluteal pain, limp, morning stiffness, deficit of external rotation of the left hip)	Paracetamol	0 weeks
Blood exams, hip US and pelvis X-ray: negative (persistence clinical findings)	Ibuprofen 30 mg/kg/die (14 days)	2 weeks
MRI a of the pelvis and left lower limb (persistence clinical findings)	US-guided left knee injection (triamcinolone hexacetonide 40 mg) + Naproxen 15 mg/kg/die (bridge therapy)	6 weeks
Diagnosis of ERA b	Sulfasalazine 40 mg/kg/die	8 weeks
POCUS: arthritis/enthesitis of the left SCJ (persistence of left gluteal pain and limping)	Sulfasalazine 50 mg/kg/die + Adalimumab 40 mg/2W	13 weeks

ER: external rotation, US: ultrasound, MRI: magnetic resonance imaging, ERA: enthesitis-related arthritis, SCJ: sternoclavicular joint, POCUS: point-of-care US.

a

Bilateral sacroiliitis, left knee synovitis, enthesitis of patellar tendon and plantar fascia.

b

Age of onset, arthritis with enthesitis, HLA-B27 positive and exclusion of other pathologies (e.g. neoplastic disorders and infections).

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Figure 3.

Whole-body MRI performed after the US examination confirmed the involvement of the left SCJ with bone marrow oedema of both the clavicular (yellow arrowhead) and sternal (white arrowhead) surfaces of the joint.

A complete clinical remission of the arthritis and enthesitis in all the anatomical regions involved was achieved after 3 months of adalimumab. The US examination during the follow-up phase was performed once a month demonstrating a progressive decrease in both, size and hypervascularisation, of the capsular and synovial hypertrophic tissue of the left SCJ.

Discussion

The SCJ is a diarthrosis playing a pivotal role as a link between the axial and peripheral skeletal system. It is a synovial joint with a double articular cavity due to the presence of a meniscoid disc made of fibrocartilaginous tissue (Figure 4). The SCJ is an unusual location of inflammatory processes in children with JIA/ERA, and in this sense, during the physical examination, it can be unintentionally overlooked.

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Figure 4.

Schematic drawing of the SCJ.

The authors searched PubMed/Medline and Web of Science for English language sources using the keywords ‘juvenile idiopathic arthritis’ and ‘sternoclavicular joint’. The search included studies published from the database’s inception to November 2023. Articles with missing patient clinical data were excluded. Interestingly, only two researches have been included in the literature review. Brijendra et al. ⁴ in 2021 published a cross-sectional study to assess the SCJ involvement in 116 JIA patients. MRI pathological changes were identified in 12.9% of the 116 JIA patients (15/116). ⁴ Specifically, bone marrow oedema, bone erosions, synovial hypertrophy and cartilage lesions were demonstrated in 15, 10, 4 and 4 patients, respectively. ⁴ The same authors reported a sensitivity and specificity of clinical examination to evaluate SCJ involvement of 55.5% and 53.3%, respectively (42 SCJs in 116 patients). ⁴ Considering the aforementioned low sensitivity and specificity of the clinical findings, the disease activity assessment using validated scales such as the juvenile spondyloarthritis disease activity index ⁷ may be not correctly quantified using the physical examination as the only diagnostic tool. Indeed, the latter index is largely used in daily practice, also/especially to manage the pharmacological therapy of JIA patients.

Huang et al. ⁸ in 2019 reported a case report of a 14-year 10-month-old boy with an unusual presentation of JIA onsetting on the SCJ. The authors performed US imaging as a first-line diagnostic tool reporting a non-specific definition of heterogeneous hypoechoic mass of 2.0 × 2.5 cm at the left sternoclavicular bump level. ⁸ Subsequently, a computed tomography scan was performed and a turbid collection within the left SCJ and irregular bone surfaces due to erosions were demonstrated. ⁸ The young patient underwent an arthrotomy, with excision of the clavicular head coupled with debridement of the left SCJ, and subsequent histological examination that excluded a malignant infiltration and confirmed the chronic inflammatory cell infiltration. ⁸ Of note, a layer-by-layer sonographic description of the different histological compartments of the pathological SCJ – cortical bone, capsule, synovial tissue and enthesis – as well as a CD assessment of its microvasculature has not been performed by Huang. ⁸ Oliver et al. ⁹ in 2022 published a detailed and standardised sonographic protocol to assess the SCJ using high-frequency transducers in B-mode; however, no description of its pathological hypervascularisation/hyperemia has been reported.

The present case report can be considered the first to accurately report the B-mode and the CD findings of a pathological SCJ in a patient with a diagnosis of ERA. Greyscale sonographic signs of anechoic intra-articular effusion, capsular bulging and hypoechoic synovial hypertrophy are well-known findings of inflammatory arthropathy.^6,10 Likewise, abnormal vascular signals of the capsule and synovial tissue on the superior aspect of SCJ in adult patients with arthritis have been previously described in the pertinent literature.^11,12 The novel sonographic sign reported in the present case report is the hypervascularisation involving the capsule–bone interface – that is, the enthesis of the joint capsule – suggesting a potential co-existence of arthritis and enthesitis of the SCJ in ERA patients. The enthesis is the anatomical area where the tendon, ligament or joint capsule inserts into the bone to transmit tensile load from soft tissues to bone.^10,13 So, for the SCJ, the term enthesis refers to the attachment sites of the capsule to the sternal and clavicular cortical bone (Figure 4). Sonographically detected enthesitis of the SCJ has been described in adult patients with ankylosing spondylitis, ¹⁴ but, to our knowledge, sonographic reports of inflammatory changes involving the SCJ enthesis in paediatric patients are lacking.

Considering the lack of a standardised and validated US surveillance programme in ERA patients, the authors performed a once-a-month sonographic examination after the diagnosis to monitor the progressive changes of B-mode and CD signs. Indeed, in the authors’ experience, 3–4 weeks are usually necessary to identify significant changes in the sonographic pattern of JIA.

The main limitation of high-resolution US imaging is the ability to accurately visualise the superior and anterior surfaces of the joint capsule but not the inferior and posterior sides of the SCJ which require panoramic imaging modalities such as the MRI.

Finally, our sonographic finding of hypervascularisation involving the capsular insertion on the clavicular side (capsular enthesitis) interestingly matches with the excision of the clavicular head performed by Huang, suggesting this anatomical site should be accurately assessed in ERA patients with clinical suspicious of SCJ involvement.

Conclusion

High-resolution US imaging is a largely available diagnostic tool in the clinical practice of rheumatologists and paediatricians that guarantees an accurate assessment of the SCJ in ERA patients. Compared to X-ray, point-of-care US allows evaluation of articular soft tissues such as the capsule and synovium with high spatial resolution and without ionising radiations; likewise, compared to MRI, it guarantees a vascular mapping of the pathological joint without using a contrast agent. In conclusion, in ERA patients with clinical findings suggestive of SCJ involvement, the high-frequency US can be considered the most suitable first-line imaging modality to assess the disease activity by combining B-mode and CD sonographic signs.