Abstract
Magnetic resonance imaging (MRI) is the imaging modality of choice for diagnosing axial spondyloarthritis (SpA) when the pelvic radiograph is normal or equivocal. Subchodral bone marrow edema (BME) is the primary feature of early SpA, although structural changes, particularly erosions, may also be seen at an early stage. It is unclear whether incorporation of structural lesions enhances the classification performance of a positive MRI definition based on BME alone. Neither spinal imaging nor contrast-enhanced imaging are useful for routine diagnostic evaluation. Fat metaplasia is a key intermediary in the pathway from inflammation to ankylosis, although the histopathology remains to be determined. Both active and structural lesions can be reliably detected and quantified on MRI. Tumor necrosis factor inhibitor therapies ameliorate inflammation; however, it is unclear whether complete suppression of inflammation is necessary to prevent structural damage. Structural lesions on MRI require further validation using computed tomography and prospective follow-up to determine their prognostic significance.
Introduction
Diagnosis of patients with axial spondyloarthritis (axSpA) covers both stages of the same disease: nonradiographic axSpA (nr-axSpA) and the “established” stage of ankylosing spondylitis (AS) . AxSpA is a chronic rheumatic inflammatory disease that primarily affects the axial skeleton; however, patients may also suffer from peripheral involvement with arthritis, enthesitis, and dactylitis , in which case, it is classified as the so-called “primarily peripheral” SpA. Pathognomonic findings of axSpA include inflammatory, osteoproliferative, or osteodestructive changes in the sacroiliac joints (SIJs) and spine. Many of these findings are a result of inflammation at the entheseal structures. Clinically, axSpA is characterized by chronic back pain, which in the majority of the cases is identified as inflammatory back pain (IBP), whereas other patients report only increased stiffness of their back . The group of SpA also shares other characteristic clinical symptoms such as anterior uveitis, psoriasis, and inflammatory bowel disease, which are considered as extra-articular manifestations of the disease. Other frequent comorbidities of SpA are osteoporosis and cardiovascular disease.
Sacroiliitis, spondylitis, aseptic spondylodiscitis, and inflammatory involvement of the posterior elements of the spine are the typical inflammatory manifestations in the axial skeleton in axSpA , which later lead to new bone formation, such as syndesmophytes and ankylosis. An estimated 15% of patients with established AS may later develop a so-called “bamboo spine” . Although all these characteristic changes occur in many patients during the course of the disease, their prevalence and the velocity of progression and severity may vary among individual patients .
The detailed pathogenic process from the inflammatory stage to the stage with more prominent structural changes in axSpA is still incompletely understood. An outstanding aspect in this regard is the concomitant occurrence of inflammatory, osteodestructive, osteoproliferative, and osteoporotic changes in the vertebral column . The involvement of the spine largely consists of new bone formation, whereas the involvement of the peripheral joints is clearly erosive.
Different imaging techniques are relevant for the diagnosis, classification, assessment of disease activity and structural damage, and prognosis of patients with axSpA; however, the capacity to detect the potential pathologies differs between the techniques. Despite technical developments, conventional radiographs (CRs) are still considered the gold standard for the assessment of structural changes in patients with axSpA . Computed tomography (CT) is useful for the detection of structural changes, particularly in the SIJ, because of its superior sensitivity and specificity compared with CRs. Nevertheless, both CR and CT cannot visualize active inflammation., MRI is the best method for the detection of inflammatory changes. The use of scintigraphy is not recommended because of its very low specificity .
For the imaging of the peripheral joints, ultrasound is being increasingly used and represents the standard imaging technique for the assessment of inflammation of the soft tissue or even erosive changes; the knowledge in this field has grown extensively in the last decade .
Overall, the different imaging techniques available for the assessment of disease-related changes in axSpA should be used in a complementary fashion and according to individual indications ( Table 1 ).
| Techniques | Inflammatory/acute changes | Structural/chronic changes | |
|---|---|---|---|
| CR | (+) | + | |
| CT | (+) | + | |
| Scintigraphy | + | – | |
| MRI | T1W | (+) | + |
| STIR/ T1/Gd-DTPA/ T2FS | ++ | (+) | |
| Ultrasound | + | (+) | |
With respect to the current classification criteria for axSpA, only changes in the SIJ are considered relevant. However, some patients may show spinal involvement in the absence of pathology in the SIJ . This topic is presently under investigation.
For study purposes, the severity of pathologic changes in the SIJ and spine of patients with axSpA can be quantified according to inflammatory and structural outcomes in the clinical trials of axSpA. Different scoring systems have been proposed for the assessment of inflammatory and structural changes in axSpA .
Importance of imaging of the sacroiliac joints in axial spondyloarthritis
Imaging of the SIJ is important for the diagnosis and classification of patients with axSpA because a vast majority of the patients show involvement of the SIJ, with an exception of those in the earliest stages of the disease. In the later stages, a certain degree of structural change in the SIJ is the definitive criterion for the classification of AS according to the 1984 modified New York criteria and classification of axSpA according to the ASAS criteria published in 2009 .
Conventional radiography
For the initial approach to a patient with suspected axSpA, X-ray imaging is the gold standard for the assessment of structural changes in the SIJ. Typical findings are sclerosis, erosions/pseudowidening, and/or bony bridges. The scoring method used for the quantification of structural changes in the SIJ in both daily practice and clinical studies has been derived from the modified New York criteria for the classification of AS . Importantly, for this evaluation, the age of the patient needs to be considered because bony changes in the SIJ may be frequently found in older populations as a consequence of local osteoarthritis. For diagnosing axSpA in early disease stages, conventional radiography has limited value because of its poor sensitivity and specificity caused by its inability to detect inflammatory activity . Routine imaging of patients with low back pain to detect chronic SIJ changes has not provided any substantial additional information in a study ; however, this may be different in younger patients with IBP and a high suspicion of axSpA . There is some evidence that structural changes in the SIJ may develop rather rapidly .
Computed tomography
CT has proven more useful than conventional radiography for the detection of structural changes in the SIJ because of its ability to provide multidimensional imaging of anatomic structures by cutting the SIJ in slices . This is of importance in the area of the SIJs because of their irregular S-shaped orientation and the partly overlapping sacral and iliac joint structures of the SIJ, which leads to a more complicated anatomy of this part of the axial skeleton .
However, similar to CRs, CT findings of sclerosis, joint space narrowing, erosions, and ankylosis may be misleading in elderly patients because subchondral sclerosis of the SIJ, particularly in the iliac part, is due to aging, which is similar to joint space narrowing .
For treatment procedures, CT-guided techniques to biopsy and injection into the SIJ have been used in experienced centers with some success .
As a general comment, the radiation exposure of CT technology needs to be taken into consideration when deciding on the imaging method to be used, even in repeated low-dose CT examinations. Therefore, CT is not recommended for the evaluation of low back pain and suspected SpA in daily routine.
Scintigraphy
Because of its ability to show enrichment in the areas of increased metabolism or inflammation, scintigraphy has been frequently used in the past to detect sacroiliac and/or spinal inflammatory activity in patients with suspected axSpA . However, its use has substantially decreased in the last few years because the sensitivity and specificity of other imaging techniques such as MRI were shown to be superior . Positive scintigraphy results in the SIJ seem to be more reliable if there is a unilateral involvement that is consistent with clinical symptoms. Because of these limitations, scintigraphy is not considered suitable for diagnosis in patients with suspected axSpA. Whether this technique can be used as a more general tool for detecting entheseal inflammation in different regions simultaneously remains to be investigated. Furthermore, similar to CT, the radiation exposure needs to be taken into consideration for the evaluation of young patients with low back pain.
Magnetic resonance imaging
One of the major advantages of MRI is the detailed anatomic and pathologic imaging quality in addition to the precise information provided on the localization of inflammation. MRI is particularly useful in detecting BME as a sign of osteitis in the axial skeleton in patients with axSpA. MRI also allows visualization of the complicated anatomy of the SIJ region, including characteristic abnormalities of the periarticular soft tissue, which is only indirectly visible by other methods ( Table 2 ). Furthermore, inflammation of the SIJ as detected by MRI correlates well with conventional histology and immunohistology and to some degree with the clinical symptoms of axSpA . MRI has also been used to detect more chronic structural changes of bone and joints. The typical structural changes in patients with axSpA are periarticular fat metaplasia, subchondral erosions, sclerosis ( Table 2 ), and bony bridges/ankylosis. In particular, the detection of fat metaplasia has raised interest because this cannot be detected by conventional X-ray imaging , although it can be predictive of future structural changes in the same location .
| Tissue | Inflammatory changes | Structural changes |
|---|---|---|
| Bone marrow | Sacroiliitis (BME/osteitis) in one or both parts of the SIJ (sacral or iliac). BME related to SpA is located periarticularly. | Subchondral sclerosis Erosions Fat metaplasia Bone bridges/ankylosis |
| Synovium | Synovitis. Depicted only by T1/Gd-DTPA sequences. STIR sequences cannot differentiate between synovitis and physiological joint fluid. Synovitis is a rare lesion. | Bone bridges/ankylosis |
| Joint capsule | Capsulitis. Comparable to synovitis. Both anterior and posterior joint capsule can be affected. | Bone bridges/ankylosis |
| Ligaments | Enthesitis, seen in the junction of ligaments and tendons to the bone. | Degeneration of ligament |
Although structural changes of the SIJ as shown by MRI are not included in the present ASAS classification criteria and the definition of a positive MRI , there is some evidence that lesions such as fat metaplasia and erosions may contribute to the diagnostic utility of MRI in axSpA . However, so far it remains unclear whether MRI can replace the CRs for the classification of axSpA as a substitute for detecting structural changes.
Importantly, and in contrast to other imaging techniques, MRI is not associated with radiation exposure. Thus, this technique is particularly favorable in young female patients, children, and patients with a past or expected history of relevant radiation exposure. However, routine access to MRI, optimal technical equipment, and skilled staff are not widely available, and the costs of MRI are higher than other imaging techniques . In addition, patients with claustrophobia, pacemakers, and metal implants cannot be examined by MRI. Furthermore, the long duration of the procedure (approximately 20–30 min) makes the technique not applicable for some patients because of intolerable pain and stiffness in the supine position .
Definition of a positive magnetic resonance imaging of the sacroiliac joint in axial spondyloarthritis
According to the ASAS definition, the hyperintense/inflammatory signal in the bone marrow near the SIJ should be preferably located in the periarticular region and should be of substantial extent. An MRI of the SIJ in patients with axSpA is considered “positive” when more than one lesion is present on one MRI slice, whereas if there is only one lesion, this should be present on at least two consecutive SIJ slices . Nevertheless, because axSpA is a chronic and constantly progressive disease, structural changes may also play an important role in the identification of patients with typical clinical symptoms in daily practice. However, because of the lack of data regarding their classification utility, structural changes are still not included in the definition of a positive MRI of the SIJ in the context of the ASAS classification criteria.
The most recently published update on this topic included structural lesions as additional findings that may contribute to a decision on whether inflammatory lesions are genuinely due to SpA . Specifically, erosions in the SIJ were considered to be important to enhance the confidence of classification of axSpA, followed by fat metaplasia and sclerosis, when not explained by other reasons such as age-related changes of the bone marrow or differential diagnoses such as osteitis condensans ilii.
Differential diagnoses for the involvement of the sacroiliac joint
BME is not a specific feature for axSpA and may also occur in other inflammatory conditions or diseases. The most important differential diagnoses for active changes in the SIJ are septic sacroiliitis, osteitis condensans ilii, and pelvic fractures. For structural changes, extensive sclerosis due to degenerative conditions or aging processes is often observed.
In the case of septic sacroiliitis, CRs are usually normal in the first weeks of disease , whereas MRI is capable of demonstrating the pathology much earlier . The major differential diagnostic criterion for axSpA is that the infection does not respect anatomical borders, leading to infiltration of the proximal parasacroiliac structures, including the iliopsoas muscle. Fractures are mainly seen as insufficiency fractures and are characterized by BME that may be similar to what is seen for sacroiliitis. A fracture line is not always visible, which may lead to a misleading interpretation of the findings, particularly when the BME looks phenotypically similar to that in axSpA.
The MRI finding of extensive sclerosis, particularly at the iliac side of the SIJ, may also be misleading. Osteitis condensans ilii, which is characterized by a triangular shaped area of sclerosis, is particularly found in women after pregnancy. It may also rarely occur in men. In diffuse idiopathic skeletal hyperostosis (DISH; Forestier’s disease), the typical findings are irregularly shaped SIJ due to various reasons including sclerosis, ossification of the joint capsule, and bony bridges, many of which may be difficult to differentiate from axSpA. However, such changes usually do not occur in young patients.
Importance of imaging of the sacroiliac joints in axial spondyloarthritis
Imaging of the SIJ is important for the diagnosis and classification of patients with axSpA because a vast majority of the patients show involvement of the SIJ, with an exception of those in the earliest stages of the disease. In the later stages, a certain degree of structural change in the SIJ is the definitive criterion for the classification of AS according to the 1984 modified New York criteria and classification of axSpA according to the ASAS criteria published in 2009 .
Conventional radiography
For the initial approach to a patient with suspected axSpA, X-ray imaging is the gold standard for the assessment of structural changes in the SIJ. Typical findings are sclerosis, erosions/pseudowidening, and/or bony bridges. The scoring method used for the quantification of structural changes in the SIJ in both daily practice and clinical studies has been derived from the modified New York criteria for the classification of AS . Importantly, for this evaluation, the age of the patient needs to be considered because bony changes in the SIJ may be frequently found in older populations as a consequence of local osteoarthritis. For diagnosing axSpA in early disease stages, conventional radiography has limited value because of its poor sensitivity and specificity caused by its inability to detect inflammatory activity . Routine imaging of patients with low back pain to detect chronic SIJ changes has not provided any substantial additional information in a study ; however, this may be different in younger patients with IBP and a high suspicion of axSpA . There is some evidence that structural changes in the SIJ may develop rather rapidly .
Computed tomography
CT has proven more useful than conventional radiography for the detection of structural changes in the SIJ because of its ability to provide multidimensional imaging of anatomic structures by cutting the SIJ in slices . This is of importance in the area of the SIJs because of their irregular S-shaped orientation and the partly overlapping sacral and iliac joint structures of the SIJ, which leads to a more complicated anatomy of this part of the axial skeleton .
However, similar to CRs, CT findings of sclerosis, joint space narrowing, erosions, and ankylosis may be misleading in elderly patients because subchondral sclerosis of the SIJ, particularly in the iliac part, is due to aging, which is similar to joint space narrowing .
For treatment procedures, CT-guided techniques to biopsy and injection into the SIJ have been used in experienced centers with some success .
As a general comment, the radiation exposure of CT technology needs to be taken into consideration when deciding on the imaging method to be used, even in repeated low-dose CT examinations. Therefore, CT is not recommended for the evaluation of low back pain and suspected SpA in daily routine.
Scintigraphy
Because of its ability to show enrichment in the areas of increased metabolism or inflammation, scintigraphy has been frequently used in the past to detect sacroiliac and/or spinal inflammatory activity in patients with suspected axSpA . However, its use has substantially decreased in the last few years because the sensitivity and specificity of other imaging techniques such as MRI were shown to be superior . Positive scintigraphy results in the SIJ seem to be more reliable if there is a unilateral involvement that is consistent with clinical symptoms. Because of these limitations, scintigraphy is not considered suitable for diagnosis in patients with suspected axSpA. Whether this technique can be used as a more general tool for detecting entheseal inflammation in different regions simultaneously remains to be investigated. Furthermore, similar to CT, the radiation exposure needs to be taken into consideration for the evaluation of young patients with low back pain.
Magnetic resonance imaging
One of the major advantages of MRI is the detailed anatomic and pathologic imaging quality in addition to the precise information provided on the localization of inflammation. MRI is particularly useful in detecting BME as a sign of osteitis in the axial skeleton in patients with axSpA. MRI also allows visualization of the complicated anatomy of the SIJ region, including characteristic abnormalities of the periarticular soft tissue, which is only indirectly visible by other methods ( Table 2 ). Furthermore, inflammation of the SIJ as detected by MRI correlates well with conventional histology and immunohistology and to some degree with the clinical symptoms of axSpA . MRI has also been used to detect more chronic structural changes of bone and joints. The typical structural changes in patients with axSpA are periarticular fat metaplasia, subchondral erosions, sclerosis ( Table 2 ), and bony bridges/ankylosis. In particular, the detection of fat metaplasia has raised interest because this cannot be detected by conventional X-ray imaging , although it can be predictive of future structural changes in the same location .
| Tissue | Inflammatory changes | Structural changes |
|---|---|---|
| Bone marrow | Sacroiliitis (BME/osteitis) in one or both parts of the SIJ (sacral or iliac). BME related to SpA is located periarticularly. | Subchondral sclerosis Erosions Fat metaplasia Bone bridges/ankylosis |
| Synovium | Synovitis. Depicted only by T1/Gd-DTPA sequences. STIR sequences cannot differentiate between synovitis and physiological joint fluid. Synovitis is a rare lesion. | Bone bridges/ankylosis |
| Joint capsule | Capsulitis. Comparable to synovitis. Both anterior and posterior joint capsule can be affected. | Bone bridges/ankylosis |
| Ligaments | Enthesitis, seen in the junction of ligaments and tendons to the bone. | Degeneration of ligament |
Although structural changes of the SIJ as shown by MRI are not included in the present ASAS classification criteria and the definition of a positive MRI , there is some evidence that lesions such as fat metaplasia and erosions may contribute to the diagnostic utility of MRI in axSpA . However, so far it remains unclear whether MRI can replace the CRs for the classification of axSpA as a substitute for detecting structural changes.
Importantly, and in contrast to other imaging techniques, MRI is not associated with radiation exposure. Thus, this technique is particularly favorable in young female patients, children, and patients with a past or expected history of relevant radiation exposure. However, routine access to MRI, optimal technical equipment, and skilled staff are not widely available, and the costs of MRI are higher than other imaging techniques . In addition, patients with claustrophobia, pacemakers, and metal implants cannot be examined by MRI. Furthermore, the long duration of the procedure (approximately 20–30 min) makes the technique not applicable for some patients because of intolerable pain and stiffness in the supine position .
Definition of a positive magnetic resonance imaging of the sacroiliac joint in axial spondyloarthritis
According to the ASAS definition, the hyperintense/inflammatory signal in the bone marrow near the SIJ should be preferably located in the periarticular region and should be of substantial extent. An MRI of the SIJ in patients with axSpA is considered “positive” when more than one lesion is present on one MRI slice, whereas if there is only one lesion, this should be present on at least two consecutive SIJ slices . Nevertheless, because axSpA is a chronic and constantly progressive disease, structural changes may also play an important role in the identification of patients with typical clinical symptoms in daily practice. However, because of the lack of data regarding their classification utility, structural changes are still not included in the definition of a positive MRI of the SIJ in the context of the ASAS classification criteria.
The most recently published update on this topic included structural lesions as additional findings that may contribute to a decision on whether inflammatory lesions are genuinely due to SpA . Specifically, erosions in the SIJ were considered to be important to enhance the confidence of classification of axSpA, followed by fat metaplasia and sclerosis, when not explained by other reasons such as age-related changes of the bone marrow or differential diagnoses such as osteitis condensans ilii.
Differential diagnoses for the involvement of the sacroiliac joint
BME is not a specific feature for axSpA and may also occur in other inflammatory conditions or diseases. The most important differential diagnoses for active changes in the SIJ are septic sacroiliitis, osteitis condensans ilii, and pelvic fractures. For structural changes, extensive sclerosis due to degenerative conditions or aging processes is often observed.
In the case of septic sacroiliitis, CRs are usually normal in the first weeks of disease , whereas MRI is capable of demonstrating the pathology much earlier . The major differential diagnostic criterion for axSpA is that the infection does not respect anatomical borders, leading to infiltration of the proximal parasacroiliac structures, including the iliopsoas muscle. Fractures are mainly seen as insufficiency fractures and are characterized by BME that may be similar to what is seen for sacroiliitis. A fracture line is not always visible, which may lead to a misleading interpretation of the findings, particularly when the BME looks phenotypically similar to that in axSpA.
The MRI finding of extensive sclerosis, particularly at the iliac side of the SIJ, may also be misleading. Osteitis condensans ilii, which is characterized by a triangular shaped area of sclerosis, is particularly found in women after pregnancy. It may also rarely occur in men. In diffuse idiopathic skeletal hyperostosis (DISH; Forestier’s disease), the typical findings are irregularly shaped SIJ due to various reasons including sclerosis, ossification of the joint capsule, and bony bridges, many of which may be difficult to differentiate from axSpA. However, such changes usually do not occur in young patients.
Imaging of the spine in axial spondyloarthritis
Spinal changes may be clinically relevant for diagnosing axSpA because they usually represent more advanced stages of the disease. However, because only 3–5% of the patients with AS were reported to have spinal changes without distinct SIJ changes , the involvement of the spine has not been part of any classification criteria for AS or axSpA so far. Another reason for this is the similarity of syndesmophytes with spondylophytes, which are of degenerative etiology but can also be found in patients with axSpA, particularly in those with longer disease duration. Thus, the clinical significance of syndesmophytes is the diagnosis of axSpA in individual patients with indefinite findings in the SIJ.
On the other hand, syndesmophytes have definite prognostic value because the presence of one syndesmophyte has been shown to significantly increase the risk for the development of more syndesmophytes . The time required for structural lesions of the spine to develop is not clearly known. Within the first 16 years of AS, such structural changes have been reported to be present in more than 50% of the patients .
Overall, both inflammatory and structural spinal changes play an important role in the evaluation of medical interventions because the effect of anti-inflammatory agents such as nonsteroidal anti-inflammatory drugs (NSAIDs) or tumor necrosis factor (TNF) blockers on spinal inflammation (BME) and new bone formation (syndesmophytes) are relevant “objective” outcomes in clinical studies on patients with axSpA.
Conventional radiographs
Similar to conventional radiography of the SIJ, CRs have a low sensitivity to detect spinal inflammation such as spondylitis, SpA, and spondylodiscitis . In addition, CRs are the gold standard for the assessment and quantification of structural spinal changes. The visualization of osteodestructive and osteoproliferative processes in the vertebral bodies is useful to assess the course of the disease and the damage that has already occurred. Spinal changes related to axSpA can be differentiated into osteodestructive (erosions) and hyperproliferative (enthesophytes, vertebral squaring, disc calcifications, spondylophytes, syndesmophytes, bony bridging, vertebral ankylosis) pathologic changes. Syndesmophytes are characterized by their typical vertical growth, which may lead to bridging phenomena in the prediscal region between the intervertebral disc and the anterior longitudinal ligament .
Magnetic resonance imaging
For the spine, MRI is considered the most sensitive method for the detection of inflammatory lesions related to axSpA . The assessment of spinal inflammation on MRI can be used as an indicator of disease activity, a response tool for biological treatment, and a possible predictor of response to therapy . Overall, spinal MRI performs best in the identification and quantification of active spinal lesions ( Table 3 ), where it has proved superior compared with other imaging techniques . T1-weighted (T1W) MRI has also been successfully used to assess structural changes ( Table 3 ) .
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