Enteropathic arthritis in the sacroiliac joint. Imaging and differential diagnosis

Enteropathic arthritis in the sacroiliac joint. Imaging and differential diagnosis

European Journal of Radiology 35 (2000) 199 – 208 www.elsevier.nl/locate/ejrad Enteropathic arthritis in the sacroiliac joint. Imaging and differenti...

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European Journal of Radiology 35 (2000) 199 – 208 www.elsevier.nl/locate/ejrad

Enteropathic arthritis in the sacroiliac joint. Imaging and differential diagnosis Adam R. Mester *, Erno3 K. Mako´, Kinga Karlinger, Tama´s Gyo¨rke, Zsolt Tarja´n, Erika Ma´rton, Katalin Kiss Semmelweis Uni6ersity, Faculty of Medicine, Department of Diagnostic Radiology and Oncotherapy, U8 lloˆi ut 78 /A, Budapest H-1082, Hungary Received 5 June 2000; received in revised form 14 June 2000; accepted 19 June 2000

Abstract Objecti6es: A new high resolution computed tomography (HRCT) scoring system of sacroiliac joint (SIJ) involvement in enteropathic arthritis is introduced. Patients and methods: SIJ’s of 100 patients were studied. A total of 25 patients presented with pain syndrome, 25 with suspicious seronegative spondylarthritis, 25 with inflammatory bowel diseases and 25 without joint or bowel diseases, as a control group. HRCT was carried out in all 100 patients. For comparison, a plain film radiography (PFR), conventional CT (slices of 10 mm) and bone scan were used. Results: Quantitative differences: In the pain syndrome group, there were no erosions identified neither intraarticular calcifications. Disc degeneration was seen in 12/25 cases. In 4/25 patients, vacuum phenomena appeared in the SIJ. In 3/25 patients, ventral capsular calcification occurred in the ventral sacroiliac ligament (anterior capsule complex). In the seronegative spondylarthritis group, 16/25 patients had positive findings, while PFR documented erosions only in 3/25 cases. In the bowel diseases group, erosions were detected in 17/25 cases with HRCT, while the plain film was positive only in three cases and in seven cases the findings were questionable. Intraarticular calcification with erosion was documented in three cases and in seven cases without erosion. The bone scan was positive in 7/25 of this cases, but in 5/7 there was mismatching with HRCT. Important new finding was the HRCT detected erosion which was not detected on BS but was obvious on Anti-Granulocyte–Antibody scintigraphy. In the control group, only degenerative changes were seen in 4/25 cases and no erosions. Conclusion: HRCT is: (1) the reliable imaging of definitive (often ‘cold stage’) sacroileitis; (2) gives optimal detection of erosion; and (3) appears to be the only method in the documentation of calcifications in the posterior ligamental portion of the SIJ. © 2000 Elsevier Science Ireland Ltd. All rights reserved. Keywords: Sacroiliac joint; Erosion; Arthritis; Crohn’s disease; Inflammatory bowel diseases

strongly connected with the anterior joint capsule. No differentiation by imaging modalities was identified in this area [1].

1. Introduction

1.1. Anatomy of the sacroiliac joint The sacroiliac joint (SIJ) is unique. The oblique joints diverge from posterior to anterior. The joint surface itself is irregular and only partially synovial. The synovial portion includes the caudal area and the frontal part of the cranial area. The dorsal part of the cranial area has no synovia and it has a strong junction with ligaments between the adjacent surfaces (interosseous sacroiliac ligaments). The ventral sacroiliac ligament is * Corresponding author. Tel.: +36-1-3343969; fax: 2100307. E-mail address: [email protected] (A.R. Mester).

+36-1-

1.2. Function of the sacroiliac joint The weight bearing function of the SIJ is complex. Some parts of the joint are compressed by the body weight and in the dorsal cranial ligamentous junction the vectors of force result in a distraction/rotation. The special composition of the SIJ allows the distribution of the body weight over a relatively large surface on the one hand and a partial elasticity during its limited movements on the other hand. The movements in the SIJ are torsion-like movements to compensate for the different superposition of shearing forces, with some

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elasticity in different postures (standing, walking, running, sitting, etc.) of the human body. Range of motion is 2 –10 mm [2].

1.3. Pathology The synovial and/or non-synovial localization of sacroileitis results in different morphology. Synovitis in the early phase can increase the distance between the calcified borders (‘radiological joint space’), e.g. knee and some other joints. This is documented with radiography in standing versus in lying positions. The etiology of this structural disintegration seen in early arthritis, is free water accumulation in the cartilage without association with proteoglycane macromolecules. With the progression of arthritis the joint space will narrow. The involvement is multilocular and the joint may appear normal, dilated or narrowed at the same time. Erosion is seen in a relatively later phase of arthritis, when focal bone loss relates to cartilage damage. Generally, erosion provokes subchondral reactive sclerosis in the adjacent bone. Both erosion and related reactive sclerosis are the conventional criteria of sacroileitis on plain film radiography (PFR). By the disease progression multilocular erosions appear in unilateral or bilateral manifestations. The manifestation of the erosions have some predictive value, e.g. unilateral (Reiter), bilateral (ankylosing spondylitis), symmetric and asymmetric (psoriasis) cases.

1.4. Clinical symptoms and classification of sacroileitis The association between colitis and arthritis was first described by White (1895). Arthritis is a common symptom in Crohn’s disease (CD), Whipple’s disease and ulcerative colitis (UC). Enteropathic arthritis belongs to the seronegative spondarthritis (SNSA) group with the characteristics of negative rheumatoid factor (RF) and absence of subcutaneous nodules. The findings are inflammatory peripheral arthritis, radiological evidence of sacroileitis with or without spondylitis, tendency to familial occurrence and frequent clinical overlap such as two or more of the followings: psoriasiform skin or nail lesions, ocular inflammation, buccal ulceration, ulceration of small or large intestine, genitourinary infection, genital ulceration, erythema nodosum, pyoderma gangrenosum, thrombophlebitis. The distinct clinical entities of the SNSA are: ankylosing spondylitis (AS), psoriatic arthritis (PA), Reiter’s disease (RD), reactive arthropathies (ReA) and enteropathic arthritis (EA). Bollow [3] suggest Seronegative and HLA B27-associated spondarthropathy (SpA) to have subcategories: ankylosing spondylitis (AS), psoriatic arthritis (PA), reactive arthritis (ReA), inflammatory bowel disease (IBD) associated arthritis and undifferentiated spondyloarthropathy (uSpA). Sacroili-

itis, an inflammatory involvement of one or both SIJ’s, is the key symptom of all spondyloarthropathies. Sets of criteria have been proposed and widely accepted in the last few years for the classification of the whole spectrum of spondyloarthropathy, including the undifferentiated forms. These classification criteria are the Amor criteria [4], the European Spondyloarthropathy Study Group criteria [4], the Bath BASRI/Ankylosing Spondylitis Radiology Index [5] and the SASSS (Stoke Ankylosing Spondylitis Spine Score [6]. In UC, peripheral arthritis occurs in 10–15% mostly in females, spondylitis in 5% mostly in males with the association of HLA-B27 positivity in 60% of cases. The knees are most commonly affected, followed by the elbow. There is a close temporal association between exacerbation of the bowel and joint disorders. In CD, peripheral arthritis occurs in 15–20%, spondylitis in 5%. Sacroiliitis is in general 10% on PFR, but data from 3 to 18% suggest that it is highly depending on the X-ray technique. In the cases of spondylitis, the most common is the involvement of cervical spine. HLA-B27 association occurs in 60–70%. In sprue syndrome/malabsorbtion, the sacroileitis is less common than in CD, but more frequent than in post–infection (reactive) arthritis ReA related arthritis. ReA in general is transient and it occurs in a number ten times smaller than in AS [7].

1.5. Imaging modalities of sacroileitis PFR is the conventional imaging of sacroileitis. While the joint is irregular and divergent from the posterior to the anterior direction, the basic supine positioning results in misleading superimposition. In this case, the erosions and irregularities of the joint space are not projected well on the film. There are two simple methods to compensate the divergent joint surfaces. The first version is that the patient lies in prone position and the X-ray tube is decreased to 90 cm. In this case, the beam divergence and the divergence of the joint are near parallel. The second version needs two exposures, and experienced technologist. The patient’s positioning in right oblique and left oblique, plus the tube angulation in caudo-cranial is a usual technique. The result is a tangential projection in optimal cases, but even small failures of positioning or individual changes can decrease the optimal level of projection. Other disadvantage is the need of two separate expositions. Anyway, there is no positioning, which could results a tangential projection of all parts of the irregular joint surface. Nuclear medicine has lower radiation exposure than plain film or CT. Quantitative measurement, e.g. sacroiliac index, helps to estimate the actual disease activity. This is a sensitive method of choice in the case of active inflammation but it is silent in inactive ‘cold’

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sacroileitis. Recently, dynamic magnetic resonance imaging (DMRI) has been found to be more sensitive and specific than a bone scan [8]. Ultrasonographic visualisation of the SIJ is limited. Ultrasonographic measurements during passive movement shows significant movements in the SIJ (\ 2 mm) in 82% of normal cases, and may be up to 10 mm in certain normal subjects [2]. Vibration test combined Doppler scan has been found helpful in predicting joint stiffness. Movements and stiffness of the SIJ is important in childbirth and in peripartum period [9]. Computed Tomography (CT) is the optimal technique in documenting bony changes. Erosions, reactive sclerosis and changes in the joint space are detected accurately even in early phases of the disease. The thinner the slices, the better resolution can be achieved. ‘Bone algorithm’ HRCT includes data collection with higher number of projections and image reconstruction with edge-enhancing filter (‘Kernel’). The radiation dose can be low as 120 kVp/175 mA/2.9 s without loosing quality. This represents less radiation exposure to the patient than with PFR [10]. Sacroiliitis is conventionally diagnosed on standard anteroposterior PFR. In AS with abnormalities suspicious to Grade 1 (out of five grades), the New York criteria CT confirms the diagnosis because it shows a higher degree of sacroiliitis. Since cartilage abnormalities precede bony changes in the early stages of the disease, MRI is superior to CT [11]. Another accepted PFR system is the (ASSS) Stoke Ankylosing Spondylitis Spine Score [6]. In the diagnosis of sacroileitis, CT is the recommended technique of choice when compared to PFR, particularly during the early onset of sacroileitis when CT is five-fold superior compared to PFR [12]. CT is helpful in differential diagnosis. Documentation of calcium pyrophosphate deposition disease (CPPD) related linear calcifications in the SIJ [13] is a characteristic feature of sacroiliac lesions in patients suffering from AS, DISH and Paget’s disease [14]. Initial involvement of only one border or new bone forming and/or destruction of the joint cartilage with complete fusion are all accurately documented if using CT. In the evaluation of SIJ aging has to be considered, e.g. narrow and less uniform joint space and subchondral sclerosis which gets wider and less uniform [15]. Certain variations, e.g. bipartite iliac bony plate, crescent-like iliac bony plate, semicircular defects at the sacral or iliac side, and ossification centers or overweight related accessory joints [16] do not mimic erosions. Sometimes complemented CT is recommended in order to document osteosclerotic bone lesions around the SIJ [17]. Certain rare conditions, such as pneumatocysts can be diagnosed by measurement of attenuation [18], or sacral stress fracture found on CT in athletic overuse [19]. In the diagnosis of hematogenous, septic

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arthritis of the SIJ BS and either CT [20], or MRI [21] are helpful. Tuberculosis in recent years has had an increasing tendency. CT imaging in these cases has a great value in early diagnosis [22]. In patients who do not respond to or do not tolerate non-steroidal antiinflammatory drugs, CT-guided corticosteroid injection into the SIJ’s has proved to be an effective therapy of florid sacroiliitis [23]. If the patient selection was appropriate, intraarticular injection of a combination of local anaesthetic and steroid gives good realties in large majority of patients [24]. Positive clinical outcome has been found in a follow up study documented with DMRI [25,26]. CT–arthrography is not part of the routine clinical practice but by using this method, three pathways of communication between the SIJ and nearby neural structures was reported [27]. MRI is the most sensitive imaging technique in the documentation of early edema. The positive predictive value in sacroiliitis (confirmed after 3 years on PR) was reported to be 60%, sensitivity 85% and specificity 47% [28]. In septic arthritis, MRI gives the early confirmation of suspected diagnosis [29], and it is useful for defining extent of infection, osteomyelitis, and abscess formation [30]. SIJ cartilage imaging has been reported to be excellent when the gradient echo with rephasing T2* was used. It is also available in low field magnets [31]. Contrast enhanced (Gd-DTPA) MRI seems to have an optimal sensitivity of 95%, which is superior to the 48% sensitivity of quantitative SI scintigraphy or the 19% sensitivity of conventional radiography for the detection and confirmation of active sacroiliitis. The specificity of MRI was reported to be 100% compared to scintigraphy (97%) and plain radiography (47%). MRI picks up an additional 75% of early cases not diagnosed by plain radiography [8]. In cases of suspected sacroileitis (clinical and/or PFR), MRI confirms the earliest diagnosis [32]. Fat suppression contrast enhanced studies showed abnormal Gd-DTPA enhancement of the SIJ’s or adjacent subchondral marrow in sacroileitis. [33]. There are better results in the subchondral lesions than with sequences without fat suppression. [34]. DMRI with T1 weighted opposed phase GE enables to detect chronic as well as acute inflammatory changes by signal-intensity curves. The potential disadvantages of this method are the dependency on the examiner, the lack of standardization, and the relatively high costs [35]. Some investigators reported CT in spondylarthropathy sacroiliitis to be significantly better than MRI, because MRI lacked sensitivity for detecting elementary lesions, particularly of the cartilage but demonstrated clearly that the earliest abnormality was edema of the subchondral bone [36].

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DMRI was identified with a positive predictive value in differentiating AS related sacroileitis of HLAB+ patients and undifferentiated sacroileitis of HLAB− patients [37]. DMRI detects morphologic changes and inflammation at the same time by documenting granulation tissue infiltrating cartilage, bone, synovium, subchondrium and the bone marrow itself [38]. A quantitative assessment of the degree of inflammation in the SIJ is available by DMRI [39].

2. Patients and methods The SIJ’s of 100 patients were studied. Study Group I included patients with pain syndrome of the SIJ area (n =25). Study Group II included patients with suspicious SNSA going to be detected or excluded from suspicion of saroileitis. Study Group III included patients with (radiological) confirmed IBD. Study Group IV included patients without joint and bowel diseases who were investigated because of other abdominal diseases. In these cases, a limited number of scans were carried out. SIJ HRCT (2-mm slice, bone algorithm image reconstruction) was carried out in all 100 patients. A comparison with PFR, conventional CT (10 mm) and groups II and III (SNSA/IBD cases), BS completed the diagnostic procedure. Other radiological investigations of the IBD patients included CT-enterography, enteroclysis and AGAb scintigraphy.

3. Results There are three levels of our results.The first is a new HRCT scoring system of the inflammatory SIJ involvement (eight categories) (see Table 1) The second level of our results include quantitative differences. In Group I (10 out of 25 patients had DISH), no erosions were detected and no intraarticular calcifications occurred. Disc degeneration was evident is 12/25 Table 1 HRCT categories in sacroileitis I (A) I (B) II (A) II (B)

SIJ\4 mm SIJB2 mm Contour irregularities Erosion (early iliac, later sacral side)

III III IV IV

Subchondral sclerosis (osteitis) ‘Spur formation’ (enchondral ossification) Transartikular bony bridges Ankylosis (synchondrosis)

(A) (B) (A) (B)

cases. In 4/25 patients, vacuum phenomena appeared in the SIJ. In 3/25 patients, ventral capsular (not real intraarticular) calcification occurred in the ventral sacroiliac ligament (VSL)-anterior capsule complex (ACC). In Group II, 16/25 patients had positive HRCT SIJ findings, while PFR documented erosions only in 3/25 cases. In 10/25 AS, 4/25 AP, in 2/25 ReA was the clinical diagnosis (undifferentiated 9/25). In Group III, 15/25 CD, 2/25 UC, 7/25 malabsorption, 1/25 low grade lymphoma was the clinical diagnosis. Erosions were detected in 17/25 cases by HRCT, while only in three cases PFR was positive, in seven cases it was doubtful. In 5/17 HRCT sacroileitis cases, the manifestation was unilateral. Intraarticular calcifications occurred in three cases with erosion together and in seven cases without erosions. The bone scan was positive in 7/25 cases, and in 5/7, there was mismatching with the HRCT. There was no positive correlation between disease duration and sacroileitis, neither age and sex. In Group IV, 4/25 cases developed non-erosive degenerative changes and in one case, triangular osteitis (‘ileitis condensans’). The third level of our results is qualitative not quantitative. The morphology of erosions seems to be specific in CD and much deeper than in other SNSA erosions. This observations are evident in a pictorial essay below.

4. Discussion The incidence of CT diagnosed SIJ in patients with low-back pain is  16% in an age group over 50 [40]. Sacroileitis was found in 13.2% in PFR of UC patients (unilateral in about the half of cases and bilateral in some smaller group [41]. In the case of UC, erosions were not as deep as erosions in CD, but more similar to SNSA manifestation in general. Classic, enteropathic, psoriatic, and reactive AS showed differences with respect to symmetry of sacroiliitis, symmetry of lumbar spinal involvement, and frequency and size of syndesmophytes. Zygoapophyseal joint involvement was more frequent in the lumbar spine in classic and enteropathic spondylitis [42]. The prevalence of radiographic evidence of sacroiliitis (grade 2 or higher) was reported to be 78% [43]. By our observations, the changes different from AS and/or SNSA/IBD related arthropathy: degenerative diseases are sclerosing but not erosive on one hand and some gas (‘vacuum symptom’) support the simple degenerative background on the other hand [44]. Our results suggest that rheumatic syndrome in IBD related arthropathies seems to be different from the classical forms of peripheral arthritis and ankylosing

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Fig. 1. Complete bony ankylosis in case of AS. The HRCT visualises irregular dilatation of the joint space behind the ankylosing new bone formation (St. IV.B.).

Fig. 4. Bilateral irregularity of the SIJ space in CD. Solitary erosion is evident on the right side on the posterior area of the synovial portion of the iliac side of the SIJ (St. II.B.).

Fig. 2. Late onset AS with multiple erosive lesions. SIJ space narrowing and dilatation, sclerosis behind the erosions are well delineated. Some spur formation is already evident (St. III.B.).

Fig. 5. Unilateral solitary deep erosion in Crohn’s disease on the sacral surface of the SIJ (St. II.B.). See AgAb scintigraphy in the Nuclear Medicine article of this issue (Fig. No 2 there).

Fig. 3. Focal dilation of the SIJ, plus unusual (8 mm) deep ‘‘fjord’’like solitary erosion, not seen in other conditions, except CD. This erosion is much deeper than the cartilage itself, and involves the bone deeper, than the usual subchondral erosive lesions in general. A real extraintestinal CD manifestation: granulomatous inflammation (St. III.A.).

Fig. 6. Early contour irregularity in the middle portion of the SIJ. Erosion is not yet observed (St. II.A.).

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Fig. 7. Early sacroileitis in Crohn’s disease. No erosions observed yet, but the irregularity of the SIJ space is evident on the right side: dilatation of the joint space (St. I.A.) and narrowing (St. I.B.). Fig. 8. Bilateral multiple erosions in UC patient. Some deep erosions with subchondral sclerosis and calcifications in the non-synovial portion of the SIJ are characteristic.

Fig. 9. Left side of the same patient with bilateral SIJ involvement. Intraarticular bony spur (IV.A) and adjacent erosion was detected in the left SIJ, with posterior ligamental calcification.

Fig. 10. Specific CD related erosion, not seen in any other SNSA sacroileitis. The solitary erosion has a very special osteochondritis dissecans-like morphology in three layers: centrally sclerotic portion, surrounded with ‘‘crescent sign’’ and asteroid lines into the deep sclerotic bone structure.

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Fig. 11. (A) Multiple deep erosions with sclerosis in CD patient (St. II.B.). Additional ligamental calcification is evident in the posterior (non-synovial) portion of the SIJ. (B) Other scan of the same patient. Osteochondritis dissecans-like lesion with three layers (see details above).

Fig. 12. Extraarticular calcification in the capsule of the synovial joint. Normal SIJ. DISH patient.

Fig. 14. Intraarticular calcifications combined with deep erosions. CD patient.

Fig. 13. (A) Extraarticular calcification in the sacrotuberous ligament. Normal SIJ. DISH patient. (B) Extraarticular calcification in the sacrotuberous ligament. Normal SIJ. DISH patient.

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Fig. 15. Intraarticular ‘‘vacuum-phenomena’’. Degenerative diseases.

Fig. 16. Spruce syndrome. Calcification in the ligamental portion of the SIJ, no erosion.

spondylitis, of degenerative, metabolic (DISH) and of SNSA and ReA. In case of IBD, there are two different mechanisms responsible for sacroileitis. Erosive (deep erosions) component is a direct manifestation of CD, some authors mention ‘metastatic Crohn’ in the case of extraintestinal manifestations. Intraarticular calcifications on the other hand seem to be related to abnormal increased permeability of bowel wall, not only present in CD, but in sprue/malabsorption syndrome also. While initial triggering of bacterial infections remains to be established in AS [38], the absence of calcifications in the ligamental portion suggests that this mechanism should be present in the overlapping cases of CD and AS. Erosions are detected equally by CT and MR and in significantly more cases than PFR. The advantage of MR is the early detection (Gd-enhancement) and the detection of subchondral erosions is improved if using CT [31]. Ventral sacroiliac ligament (VSL) – anterior capsule complex (ACC) can be documented with MRI [1], but CT is superior in detecting calcifications. This type of calcification was not observed in our SNSA or IBD patients, but detected in DISH patients instead. Calcifications in DISH are different to posterior intraarticular calcifications often detected in IBD patients. Clinical and radiological characteristic association with HLA B27 in (IBD patients and subclinical sacroileitis was reported by Queiro Silva [45], which was generally grade 2 (New York criteria) unilateral sacroileitis. They did not find a correlation between sacroileitis and IBDP type, extradigestive symptoms, disease duration sex, or peripheral arthritis. The frequency of HLA B27 in the PFR sacroileitis group was 20%. The demographic, clinical, and radiological characteristics were collected. The radiological examination

included PA and lateral views for the dorso-lumbar, and three views (Ferguson, right and left oblique views) for the SIJ’s. The HLA B27 allele distribution was analysed in the 62 patients and in 80 healthy controls. The modified New York criteria, Amor criteria, and European Spondyloarthropathy Study Group criteria were evaluated. A high frequency of asymptomatic sacroileitis in patients with IBD was detected. They propose the term of ‘Silent Axial Arthropathy’ to define this category of patients and consider this to be a third form of rheumatic syndrome in IBD, different from the classical forms of peripheral arthritis and ankylosing spondylitis. HRCT is superior to PFR not only in the case of SIJ, but also in the lung parenchyma in AS patients. In 70%, AS patients had interstitial lung disease confirmed by HRCT of the lung, while plain radiography was abnormal in only 20% of the patients [46]. 5. Conclusion Imaging of sacroileitis in the early/transient phase is optimal if BS and/or MRI are used. HRCT is the safe imaging of definitive sacroileitis, while remaining positive in the ‘cold’ stage also. Detection of erosions is optimal if using HRCT. The only method to visualise calcifications in the posterior (ligamental) portion of the SIJ is HRCT (Figs. 1–16). References [1] Jaovisidha S, Ryu KN, De Maeseneer M, Haghighi P, Goodwin D, Sartoris DJ, Resnick D. Ventral sacroiliac ligament. Anatomic and pathologic considerations. Invest Radiol 1996;31(8):532– 41.

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