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Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values
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ARTICLE IN PRESS European Journal of Radiology xxx (2013) xxx–xxx
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Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values Esin Gezmis, Fuldem Y. Donmez ∗ , Muhtesem Agildere Baskent University, Faculty of Medicine, Department of Radiology, Turkey
a r t i c l e
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Article history: Received 3 January 2013 Received in revised form 7 June 2013 Accepted 17 August 2013 Keywords: DWI Seronegative spondyloarthropathies Sacroiliitis
a b s t r a c t Purpose: Sacroiliitis is one of the diagnostic criteria of seronegative SpA. The purpose of our study is to show the signal characteristics of the sacral and iliac surfaces by DWI which may contribute in early diagnosis of sacroiliitis and investigate the correlation between ADC values and clinical and laboratory parameters. Materials and methods: 62 patients with inflammatory low back pain, with a history or suspect of seronegative SpA are enrolled into the study. 40 age and sex-matched subjects without SpA constituted the control group. After obtaining routine T1 and T2 weighted sequences, echo planar imaging at b values of 0, 400 and 800 was performed. ADC values on both surfaces of the both sacroiliac joints were measured in all subjects. The CRP and sedimentation results and the presence of arthritis and enthesitis were also correlated with the ADC values. Results: ADC values on both surfaces of the both sacroiliac joints were found 0.23 × 10−3 mm2 /sn in the control group. In the patient group, mean ADC value of 0.48 × 10−3 mm2 /sn was obtained (p < 0.001), which was statistically significant, compatible with the increased diffusion due to medullary edema in early sacroiliitis. There was a slight correlation between CRP and ADC values; presumed to be showing the relation between the activity of the disease and the active inflammation on DWI. There was no correlation between arthritis and enthesitis and the ADC values (p > 0.001). Conclusion: DWI, by measuring ADC values, adds significant information in the early diagnosis of sacroiliitis and may help to evaluate the efficiency of the treatment. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Seronegative spondyloarthropathies (SpA), including ankylosing spondylitis, psoriatic arthritis, Reiter syndrome and enteropathic arthritis are a heterogeneous group of diseases which have an unknown origin and have no relationship with rheumatoid factor. In the axial skeleton, sacroiliac joints are primarily affected, moreover, sacroiliitis is one of the major diagnostic criteria in this group of patients. The presenting symptoms are back or hip pain. Since differentiating mechanical back pain from inflammatory pain is clinically difficult, imaging aids in diagnosis. Plain radiographs are the first imaging method to prefer, however it takes a long time
for the positive findings to appear on plain films therefore, they are insensitive. Even some clinical criteria such as ESSG, ASAS and modified New York criteria may delay the diagnosis. At this point MRI meets the needs of the clinician, and is now among the diagnostic criteria [1]. MRI may show sacroiliitis despite negative laboratory findings [2]. Lately, diffusion-weighted MRI (DW-MRI) promises to show the early changes in microscopical movement of the water molecules, hence early sacroiliitis. In this study, we aimed to assess whether DW-MRI can help to show the early subchondral edema in the sacroiliac joints and investigate the correlation between the ADC values and the clinical and laboratory findings such as ESR, CRP and HLA-B27. 2. Materials and methods
Abbreviations: SpA, spondyloarthropathy; ESSG, European Spondyloarthropathy Study Group; ASAS, Assessment of SpondyloArthritis International Society; ESR, erythrocyte sedimentation rate; CRP, C-reactive protein. ∗ Corresponding author at: Baskent University, Department of Radiology, Fevzi Cakmak Caddesi 06490, Bahcelievler, Ankara, Turkey. Tel.: +90 312 2235417; fax: +90 312 2237333. E-mail address: [email protected] (F.Y. Donmez).
2.1. Subjects Sixty-two patients with clinically definite SpA who were admitted to the rheumatology clinic between May 2010 and August 2011 (27 men, 35 women; mean age, 39 years; range 16–62 years) were
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Please cite this article in press as: Gezmis E, et al. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol (2013), http://dx.doi.org/10.1016/j.ejrad.2013.08.032
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Fig. 1. The DWI and ADC map of a patient who had no signal abnormality (a, b). The ADC measurements are done in patients who did not show any pathologic signal intensity as shown (c).
enrolled into the study and constituted Group 1. Control population consisted of the subjects who had no inflammatory back pain or suspicious physical examination for SpA, with normal laboratory findings such as ESR and CRP and MRI within normal limits (40 patients, 16 men, 24 women; mean age 33.3; range, 20–60 years). According to the institutional guidelines, all subjects gave informed written consent approved by our institutional review board before MRI.
2.2. MRI acquisition MRI studies were performed on two 1.5 Tesla systems (Avanto and Symphony, Siemens, Erlangen, Germany). Standard protocol for sacroiliac joints including STIR (TR/TE/TI: 4360/58/160 ms; matrix: 320 × 192; NEX: 3; slice thickness: 4 mm), T1-weighted (TR/TE: 436/10 ms; matrix: 384 × 269; NEX: 2; slice thickness: 4 mm), fat-saturated T1-weighted (TR/TE: 525/10; matrix: 384 × 200; NEX: 3; slice thickness: 4 mm) and T2-weighted (TR/TE: 4280/94 ms; matrix: 512 × 256; NEX: 2; slice thickness: 4 mm) in coronal oblique and axial planes was performed with spinal coil. FOV was 230 mm for axial and 250 mm for coronal oblique planes. Echo-planar images were obtained with diffusion gradients in the x, y, z planes at b values of 0, 400 and 800 (TR/TE: 6000/90 ms; matrix: 192 × 153; NEX: 2; slice thickness: 4 mm). Apparent diffusion coefficient (ADC) maps were automatically created.
2.3. Image processing and analysis An ROI (region of interest) of 75–80 mm [2] was placed on superior, middle and inferior subchondral areas of iliac and sacral sides of both sacroiliac joints (total of 12) and these ADC measurements are made in both patient and control group (Fig. 1). The areas which were hypointense on T1-weighted and hyperintense on T2-weighted images were determined to be bone marrow edema, and ADC measurements from these areas (Fig. 2) are compared to the ADC values of the equivalent areas of control subjects. All MRI examinations were reviewed at a Workstation for qualitative and quantitative evaluation by two radiologists on consensus. The ADC values of two groups were compared by using independent samples t test. The CRP and ESR values of the patients at the time of their admission with the complaint of back pain were noted and these values were correlated with the ADC values of the control subjects. The correlation between sedimentation rate and ADC and CRP values and ADC values were evaluated by Spearman Correlation analysis. HLA-B27 was also sought in 17 of the patients. Patients with SpA were also assessed for the clinical findings such as arthritis, enthesitis, uveitis, dactylitis, Crohn or ulcerative colitis diseases, urethritis and family history of SpA. The number of patients with uveitis (n:6), dactylitis (n:2), Crohn or ulcerative
Please cite this article in press as: Gezmis E, et al. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol (2013), http://dx.doi.org/10.1016/j.ejrad.2013.08.032
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Fig. 2. The DWI and ADC map of a patient who had increased signal intensity on both sides of the left sacroiliac joint (a, b). The ADC values are obtained from the pathologic signal intensity areas as shown (c).
colitis diseases (n:1), urethritis (n:4) and family history of SpA (n:5) was so small to make a reliable statistical analysis. The presence of the arthritis and enthesitis were compared to the ADC values. 3. Results Both of the groups were homogeneous, there was no difference in the gender and age distribution statistically. Of the 62 patients with inflammatory back pain, 12 patients had ankylosing spondylitis, 1 patient had juvenile ankylosing spondylitis, 1 patient had psoriatic arthritis and 48 patients were diagnosed as undifferentiated seronegative spondyloarthropathy and their treatments were started. 29 patients had subchondral edema on sacroiliac MRI. Eleven patients had edema on right and 15 patients had edema on left sacral side of the joint; 14 patients had edema on the right and 11 patients had edema on the left iliac side of the joint. Mean ADC values on the right sacral bone marrow edema in 11 patients and on the left sacral bone marrow edema in 15 patients were calculated as 0.90 × 10−3 mm2 /sn and 0.89 × 10−3 mm2 /sn respectively
(ADC value in the same localization of the right and left sacral bone in control group was 0.23 × 10−3 mm2 /sn). Mean ADC values on the right iliac bone marrow edema in 14 patients and on the left iliac bone marrow edema in 11 patients were calculated as 0.84 × 10−3 mm2 /sn and 0.82 × 10−3 mm2 /sn respectively (ADC value in the same localization of the right and left iliac bone in control group was found as 0.22 × 10−3 mm2 /sn). The differences in ADC values between Group 1 and Group 2 were statistically significant (p < 0.001). ADC values from the normal appearing areas, showing no edema were calculated at 3 points (superior, middle and inferior) on both sacral and iliac surfaces of both sacroiliac joints. The calculated ADC values on the right sacral, left sacral and right iliac and left iliac surfaces of the patients and control group are tabulated in Tables 1, 2, 3 and 4 respectively. As shown in the tables, the values obtained from the patient and control group are found statistically different (p < 0.001). The mean value of the abovementioned 12 calculations were found 0.48 × 10−3 mm2 /sn in Group 1 and 0.23 × 10−3 mm2 /sn in Group 2, which is statistically significant (p < 0.001).
Please cite this article in press as: Gezmis E, et al. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol (2013), http://dx.doi.org/10.1016/j.ejrad.2013.08.032
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Table 1 The ADC values of the patient and control groups on the right sacral bone. Right sacral ADC
Patient (n = 62)Mean ± SD
Control (n = 40)Mean ± SD
p
Superior Middle Inferior
0.47 × 10- 3 ± 0.19 0.47 × 10- 3 ± 0.18 0.53 × 10- 3 ± 0.22
0.20 × 10- 3 ± 0.07 0.24 × 10- 3 ± 0.09 0.26 × 10- 3 ± 0.09
<0.001 <0.001 <0.001
Table 2 The ADC values of the patient and control groups on the left sacral bone. Left sacral ADC
Patient (n = 62)Mean ± SD
Control (n = 40)Mean ± SD
p
Superior Middle Inferior
0.45 × 10- 3 ± 0.13 0.47 × 10- 3 ± 0.20 0.50 × 10- 3 ± 0.13
0.21 × 10- 3 ± 0.08 0.23 × 10- 3 ± 0.08 0.26 × 10- 3 ± 0.09
<0.001 <0.001 <0.001
Laboratory parameters in diagnosis of SpA such as ESR, CRP and HLA-B27 were also evaluated. ESR was found high in 20 patients and CRP was higher than normal in 11 patients. HLA-B27 was found positive in 5 of 17 patients who had the HLA test. The number of patients with HLA-B27 test was so small to make a statistical analysis, therefore it was not correlated with the ADC values. The correlation between ESR and ADC was not found significant (p > 0.001). However, slight correlation was found between the CRP values and ADC values (p < 0.001). In Group 1, ADC values of 21 patients who had clinical findings of arthritis on other joints of the body were compared to the ADC values of the 41 patients who lacked arthritis, and no significant difference was found statistically (Table 5). ADC values of 21 patients who had clinical findings of enthesitis were compared to the ADC values of the 41 patients who did not have enthesitis, and no correlation was found statistically (Table 6). 4. Discussion Diagnosing sacroiliitis in patients with SpA is important in planning the treatment and for follow-up protocols [3,4]. Therefore, early diagnosis of sacroiliitis is crucial to prevent the possible complications in the late period of the disease [5]. However, clinical evaluation is limited; imaging is needed in most of the cases [6]. Although radiographs are easily available initial imaging method, there is a relatively long period between the occurrence of the symptoms and appearance of the findings on the radiographs. Moreover, the oblique course of the sacroiliac joint, the superposition of the sacral and iliac bones and wavy nature of the joint make the interpretation harder [6–8]. MRI can show the ligamentous and synovial components far better than any of the imaging methods and can depict the erosive or sclerotic changes, pathologies of the capsule and synovium, chondral lesions and marrow diseases [9]. There are some studies emphasizing on the use of contrast media in increasing the sensitivity of MRI for diagnosing activation of the disease [10]. Ability of MRI in showing active inflammation is
also another advantage as it is an important criterion in treatment planning. Therefore, MRI findings take place in the new diagnostic criteria of SpA according to ASAS, which has the highest sensitivity among all diagnostic criteria since June 2009 [1]. Although routine MRI has high sensitivity in showing the abovementioned abnormalities related to the sacroiliac joints and the bone marrow, these findings are mostly nonspecific. DWI-MRI has the potential of increasing the specificity of MRI [11]. The ADC value, a diffusivity index, is a quantitative marker for tissue characterization. The contribution of T2-weighting to DWI may cause false positive results as diffusion restriction, therefore qualitative assessment may not be efficient, and quantitative measurements should be made. There are some studies on differentiating benign and pathologic vertebra fractures by DWI and ADC measurements, which revealed lower ADC values for pathologic fractures [12,13]. However, despite quantitative measurements, DWI-MRI has its own limitations. For example, although it is mostly successful in differentiating benign and malignant fractures, there is significant overlap of ADC values in some cases. Differentiating treatment response from residual spinal metastases is mostly reliable but limited use is reported for evaluation of sclerotic bone metastases. Overlapping spectrum of DWI-MRI findings are also found for bone and soft tissue tumors and bone infection, limiting its clinical value [14]. We performed MRI and DWI in 62 patients with SpA and 40 subjects in the control group. The mean ADC values of the subchondral bone on both sacral and iliac joints are found as 0.23 × 10−3 mm2 /sn. Vertebral marrow has 20–70% fat component, which has low diffusivity, resulting in low ADC values. In other studies, vertebral ADC values were found ranging between 0.15 × 10−3 mm2 /sn and 0.59 × 10−3 mm2 /sn [15–17]. These low values are due to the slow diffusion of water molecules bounded to the fat molecules of the yellow marrow. Dietrich et al. [18] performed DWI with b value of 50 and 500 sn/mm2 , and found mean ADC value of 0.3 × 10−3 mm2 /sn, whereas Chan et al. [15] performed DWI at b value of only 1000 sn/mm2 , and reported the mean
Table 3 The ADC values of the patient and control groups on the right iliac bone. Right iliac ADC
Patient (n = 62)Mean ± SD
Control (n = 40)Mean ± SD
p
Superior Middle Inferior
0.47 × 10- 3 ± 0.19 0.48 × 10- 3 ± 0.18 0.54 × 10- 3 ± 0.22
0.20 × 10- 3 ± 0.07 0.24 × 10- 3 ± 0.09 0.26 × 10- 3 ± 0.09
<0.001 <0.001 <0.001
Table 4 The ADC values of the patient and control groups on the left iliac bone. Left iliac ADC
Patient (n = 62)Mean ± SD
Control (n = 40)Mean ± SD
p
Superior Middle Inferior
0.45 × 10- 3 ± 0.18 0.47 × 10- 3 ± 0.18 0.49 × 10- 3 ± 0.28
0.19 × 10- 3 ± 0.06 0.23 × 10- 3 ± 0.09 0.24 × 10- 3 ± 0.08
<0.001 <0.001 <0.001
Please cite this article in press as: Gezmis E, et al. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol (2013), http://dx.doi.org/10.1016/j.ejrad.2013.08.032
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Table 5 The comparison of the ADC values of patients who had arthritis and who did not have arthritis. ADC
Arthritis (−) (n = 41)Mean ± SD
Arthritis (+) (n = 21)Mean ± SD
p
R Sacral Superior R Sacral Middle R Sacral Inferior R Iliac Superior R Iliac Middle R Iliac Inferior L Sacral Superior L Sacral Middle L Sacral Inferior L Iliac Superior L Iliac Middle L Iliac Inferior
0.44 × 10- 3 0.47 × 10- 3 0.52 × 10- 3 0.46 × 10- 3 0.46 × 10- 3 0.53 × 10- 3 0.45 × 10- 3 0.48 × 10- 3 0.49 × 10- 3 0.44 × 10- 3 0.48 × 10- 3 0.50 × 10- 3
0.47 × 10- 3 0.50 × 10- 3 0.48 × 10- 3 0.50 × 10- 3 0.50 × 10- 3 0.55 × 10- 3 0.44 × 10- 3 0.47 × 10- 3 0.51 × 10- 3 0.46 × 10- 3 0.46 × 10- 3 0.47 × 10- 3
0.341 0.693 0.120 0.587 0.672 0.994 0.624 0.246 0.760 0.818 0.225 0.301
± ± ± ± ± ± ± ± ± ± ± ±
0.11 0.12 0.15 0.12 0.12 0.21 0.14 0.18 0.13 0.16 0.13 0.17
± ± ± ± ± ± ± ± ± ± ± ±
0.10 0.16 0.10 0.29 0.26 0.25 0.12 0.24 0.13 0.22 0.26 0.20
Table 6 The comparison of the ADC values of patients who had enthesitis and who did not have enthesitis. ADC
Enthesitis (−) (n = 41)Mean ± SD
Enthesitis (+) (n = 21)Mean ± SD
p
R Sacral Superior R Sacral Middle R Sacral Inferior R Iliac Superior R Iliac Middle R Iliac Inferior L Sacral Superior L Sacral Middle L Sacral Inferior L Iliac Superior L Iliac Middle L Iliac Inferior
0.45 × 10- 3 0.50 × 10- 3 0.52 × 10- 3 0.49 × 10- 3 0.48 × 10- 3 0.57 × 10- 3 0.44 × 10- 3 0.49 × 10- 3 0.51 × 10- 3 0.46 × 10- 3 0.49 × 10- 3 0.51 × 10- 3
0.46 × 10- 3 0.44 × 10- 3 0.47 × 10- 3 0.44 × 10- 3 0.46 × 10- 3 0.46 × 10- 3 0.46 × 10- 3 0.43 × 10- 3 0.48 × 10- 3 0.43 × 10- 3 0.44 × 10- 3 0.46 × 10- 3
0.905 0.051 0.086 0.597 0.935 0.056 0.518 0.231 0.499 0.958 0.345 0.699
± ± ± ± ± ± ± ± ± ± ± ±
0.11 0.14 0.15 0.22 0.21 0.25 0.14 0.23 0.14 0.21 0.21 0.21
ADC value as 0.23 × 10−3 mm2 /sn. Bozgeyik et al. [19] obtained DWI at b values of 100, 600 and 1000 and calculated the mean ADC value as 0.67 × 10−3 mm2 /sn. The difference of ADC values in different studies was tributed to the different imaging techniques and b values. Age is also an important factor affecting the vertebral marrow component. By increasing age, osteoporotic changes may cause decrease in ADC values. The higher ADC values reported in the study of Bozgeyik et al. may be due to the younger study population (mean age 26). The mean ADC value of 0.86 × 10−3 mm2 /sn obtained from the hyperintense bone marrow areas is significantly higher than the control group. Moreover, the mean ADC value of 0.48 × 10−3 mm2 /sn obtained from the normal appearing subchondral areas adjacent to the sacroiliac joint is also significantly higher than the control group. This is thought to be due to the increase of the movement of the water molecules because of the bone marrow edema. Although there may not be signal alterations, quantitative measurements also show that there is increased diffusion in normal appearing areas. Therefore, in case of clinically diagnosed SpA, after excluding other pathologies both clinically and based on conventional MRI sequences, DWI images should be evaluated visually firstly, which may give the idea of increased diffusion in presence of high signal on ADC map. However, absence of signal alterations at first look should not deter the radiologist from the idea of possible sacroiliitis and therefore quantitative ADC measurements should be done. CRP and ESR are laboratory parameters of inflammation; there are some studies reporting that the increase in CRP and ESR may be used as a marker of inflammation and activity of the disease. In a study of Won-Hee Jee et al. [20], a correlation between ESR with CRP values and synovial contrast enhancement on MRI was reported. However, in a study by Puhakka et al. [2], there was no abnormality in the CRP values in patients who had sacroiliitis on MRI. To our knowledge, there is no other study searching any correlation between the ADC values and laboratory parameters. Although the number of patients is low, the findings in our study show that a
± ± ± ± ± ± ± ± ± ± ± ±
0.10 0.09 0.10 0.12 0.10 0.13 0.11 0.11 0.14 0.09 0.10 0.10
laboratory marker, CRP and an imaging marker, ADC may correlate well on the activity of the disease. The presence of clinical findings of SpA such as arthritis and enthesitis did not show any correlation with ADC values, however, the number of patients was not sufficient to make a statistical analysis. The reason of non-correlation may also be that most of the patients with arthritis and enthesitis were in the chronic stage of the disease. In conclusion, DWI is a sensitive, fast sequence which can help to differentiate normal and pathologic bone marrow areas by ADC measurements which cannot be visually evaluated. It can be used to diagnose early sacroiliitis in SpA patients and follow the treatment effects.
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Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values Esin Gezmis, Fuldem Y. Donmez ∗ , Muhtesem Agildere Baskent University, Faculty of Medicine, Department of Radiology, Turkey
a r t i c l e
i n f o
Article history: Received 3 January 2013 Received in revised form 7 June 2013 Accepted 17 August 2013 Keywords: DWI Seronegative spondyloarthropathies Sacroiliitis
a b s t r a c t Purpose: Sacroiliitis is one of the diagnostic criteria of seronegative SpA. The purpose of our study is to show the signal characteristics of the sacral and iliac surfaces by DWI which may contribute in early diagnosis of sacroiliitis and investigate the correlation between ADC values and clinical and laboratory parameters. Materials and methods: 62 patients with inflammatory low back pain, with a history or suspect of seronegative SpA are enrolled into the study. 40 age and sex-matched subjects without SpA constituted the control group. After obtaining routine T1 and T2 weighted sequences, echo planar imaging at b values of 0, 400 and 800 was performed. ADC values on both surfaces of the both sacroiliac joints were measured in all subjects. The CRP and sedimentation results and the presence of arthritis and enthesitis were also correlated with the ADC values. Results: ADC values on both surfaces of the both sacroiliac joints were found 0.23 × 10−3 mm2 /sn in the control group. In the patient group, mean ADC value of 0.48 × 10−3 mm2 /sn was obtained (p < 0.001), which was statistically significant, compatible with the increased diffusion due to medullary edema in early sacroiliitis. There was a slight correlation between CRP and ADC values; presumed to be showing the relation between the activity of the disease and the active inflammation on DWI. There was no correlation between arthritis and enthesitis and the ADC values (p > 0.001). Conclusion: DWI, by measuring ADC values, adds significant information in the early diagnosis of sacroiliitis and may help to evaluate the efficiency of the treatment. © 2013 Elsevier Ireland Ltd. All rights reserved.
1. Introduction Seronegative spondyloarthropathies (SpA), including ankylosing spondylitis, psoriatic arthritis, Reiter syndrome and enteropathic arthritis are a heterogeneous group of diseases which have an unknown origin and have no relationship with rheumatoid factor. In the axial skeleton, sacroiliac joints are primarily affected, moreover, sacroiliitis is one of the major diagnostic criteria in this group of patients. The presenting symptoms are back or hip pain. Since differentiating mechanical back pain from inflammatory pain is clinically difficult, imaging aids in diagnosis. Plain radiographs are the first imaging method to prefer, however it takes a long time
for the positive findings to appear on plain films therefore, they are insensitive. Even some clinical criteria such as ESSG, ASAS and modified New York criteria may delay the diagnosis. At this point MRI meets the needs of the clinician, and is now among the diagnostic criteria [1]. MRI may show sacroiliitis despite negative laboratory findings [2]. Lately, diffusion-weighted MRI (DW-MRI) promises to show the early changes in microscopical movement of the water molecules, hence early sacroiliitis. In this study, we aimed to assess whether DW-MRI can help to show the early subchondral edema in the sacroiliac joints and investigate the correlation between the ADC values and the clinical and laboratory findings such as ESR, CRP and HLA-B27. 2. Materials and methods
Abbreviations: SpA, spondyloarthropathy; ESSG, European Spondyloarthropathy Study Group; ASAS, Assessment of SpondyloArthritis International Society; ESR, erythrocyte sedimentation rate; CRP, C-reactive protein. ∗ Corresponding author at: Baskent University, Department of Radiology, Fevzi Cakmak Caddesi 06490, Bahcelievler, Ankara, Turkey. Tel.: +90 312 2235417; fax: +90 312 2237333. E-mail address: [email protected] (F.Y. Donmez).
2.1. Subjects Sixty-two patients with clinically definite SpA who were admitted to the rheumatology clinic between May 2010 and August 2011 (27 men, 35 women; mean age, 39 years; range 16–62 years) were
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Fig. 1. The DWI and ADC map of a patient who had no signal abnormality (a, b). The ADC measurements are done in patients who did not show any pathologic signal intensity as shown (c).
enrolled into the study and constituted Group 1. Control population consisted of the subjects who had no inflammatory back pain or suspicious physical examination for SpA, with normal laboratory findings such as ESR and CRP and MRI within normal limits (40 patients, 16 men, 24 women; mean age 33.3; range, 20–60 years). According to the institutional guidelines, all subjects gave informed written consent approved by our institutional review board before MRI.
2.2. MRI acquisition MRI studies were performed on two 1.5 Tesla systems (Avanto and Symphony, Siemens, Erlangen, Germany). Standard protocol for sacroiliac joints including STIR (TR/TE/TI: 4360/58/160 ms; matrix: 320 × 192; NEX: 3; slice thickness: 4 mm), T1-weighted (TR/TE: 436/10 ms; matrix: 384 × 269; NEX: 2; slice thickness: 4 mm), fat-saturated T1-weighted (TR/TE: 525/10; matrix: 384 × 200; NEX: 3; slice thickness: 4 mm) and T2-weighted (TR/TE: 4280/94 ms; matrix: 512 × 256; NEX: 2; slice thickness: 4 mm) in coronal oblique and axial planes was performed with spinal coil. FOV was 230 mm for axial and 250 mm for coronal oblique planes. Echo-planar images were obtained with diffusion gradients in the x, y, z planes at b values of 0, 400 and 800 (TR/TE: 6000/90 ms; matrix: 192 × 153; NEX: 2; slice thickness: 4 mm). Apparent diffusion coefficient (ADC) maps were automatically created.
2.3. Image processing and analysis An ROI (region of interest) of 75–80 mm [2] was placed on superior, middle and inferior subchondral areas of iliac and sacral sides of both sacroiliac joints (total of 12) and these ADC measurements are made in both patient and control group (Fig. 1). The areas which were hypointense on T1-weighted and hyperintense on T2-weighted images were determined to be bone marrow edema, and ADC measurements from these areas (Fig. 2) are compared to the ADC values of the equivalent areas of control subjects. All MRI examinations were reviewed at a Workstation for qualitative and quantitative evaluation by two radiologists on consensus. The ADC values of two groups were compared by using independent samples t test. The CRP and ESR values of the patients at the time of their admission with the complaint of back pain were noted and these values were correlated with the ADC values of the control subjects. The correlation between sedimentation rate and ADC and CRP values and ADC values were evaluated by Spearman Correlation analysis. HLA-B27 was also sought in 17 of the patients. Patients with SpA were also assessed for the clinical findings such as arthritis, enthesitis, uveitis, dactylitis, Crohn or ulcerative colitis diseases, urethritis and family history of SpA. The number of patients with uveitis (n:6), dactylitis (n:2), Crohn or ulcerative
Please cite this article in press as: Gezmis E, et al. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol (2013), http://dx.doi.org/10.1016/j.ejrad.2013.08.032
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Fig. 2. The DWI and ADC map of a patient who had increased signal intensity on both sides of the left sacroiliac joint (a, b). The ADC values are obtained from the pathologic signal intensity areas as shown (c).
colitis diseases (n:1), urethritis (n:4) and family history of SpA (n:5) was so small to make a reliable statistical analysis. The presence of the arthritis and enthesitis were compared to the ADC values. 3. Results Both of the groups were homogeneous, there was no difference in the gender and age distribution statistically. Of the 62 patients with inflammatory back pain, 12 patients had ankylosing spondylitis, 1 patient had juvenile ankylosing spondylitis, 1 patient had psoriatic arthritis and 48 patients were diagnosed as undifferentiated seronegative spondyloarthropathy and their treatments were started. 29 patients had subchondral edema on sacroiliac MRI. Eleven patients had edema on right and 15 patients had edema on left sacral side of the joint; 14 patients had edema on the right and 11 patients had edema on the left iliac side of the joint. Mean ADC values on the right sacral bone marrow edema in 11 patients and on the left sacral bone marrow edema in 15 patients were calculated as 0.90 × 10−3 mm2 /sn and 0.89 × 10−3 mm2 /sn respectively
(ADC value in the same localization of the right and left sacral bone in control group was 0.23 × 10−3 mm2 /sn). Mean ADC values on the right iliac bone marrow edema in 14 patients and on the left iliac bone marrow edema in 11 patients were calculated as 0.84 × 10−3 mm2 /sn and 0.82 × 10−3 mm2 /sn respectively (ADC value in the same localization of the right and left iliac bone in control group was found as 0.22 × 10−3 mm2 /sn). The differences in ADC values between Group 1 and Group 2 were statistically significant (p < 0.001). ADC values from the normal appearing areas, showing no edema were calculated at 3 points (superior, middle and inferior) on both sacral and iliac surfaces of both sacroiliac joints. The calculated ADC values on the right sacral, left sacral and right iliac and left iliac surfaces of the patients and control group are tabulated in Tables 1, 2, 3 and 4 respectively. As shown in the tables, the values obtained from the patient and control group are found statistically different (p < 0.001). The mean value of the abovementioned 12 calculations were found 0.48 × 10−3 mm2 /sn in Group 1 and 0.23 × 10−3 mm2 /sn in Group 2, which is statistically significant (p < 0.001).
Please cite this article in press as: Gezmis E, et al. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol (2013), http://dx.doi.org/10.1016/j.ejrad.2013.08.032
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Table 1 The ADC values of the patient and control groups on the right sacral bone. Right sacral ADC
Patient (n = 62)Mean ± SD
Control (n = 40)Mean ± SD
p
Superior Middle Inferior
0.47 × 10- 3 ± 0.19 0.47 × 10- 3 ± 0.18 0.53 × 10- 3 ± 0.22
0.20 × 10- 3 ± 0.07 0.24 × 10- 3 ± 0.09 0.26 × 10- 3 ± 0.09
<0.001 <0.001 <0.001
Table 2 The ADC values of the patient and control groups on the left sacral bone. Left sacral ADC
Patient (n = 62)Mean ± SD
Control (n = 40)Mean ± SD
p
Superior Middle Inferior
0.45 × 10- 3 ± 0.13 0.47 × 10- 3 ± 0.20 0.50 × 10- 3 ± 0.13
0.21 × 10- 3 ± 0.08 0.23 × 10- 3 ± 0.08 0.26 × 10- 3 ± 0.09
<0.001 <0.001 <0.001
Laboratory parameters in diagnosis of SpA such as ESR, CRP and HLA-B27 were also evaluated. ESR was found high in 20 patients and CRP was higher than normal in 11 patients. HLA-B27 was found positive in 5 of 17 patients who had the HLA test. The number of patients with HLA-B27 test was so small to make a statistical analysis, therefore it was not correlated with the ADC values. The correlation between ESR and ADC was not found significant (p > 0.001). However, slight correlation was found between the CRP values and ADC values (p < 0.001). In Group 1, ADC values of 21 patients who had clinical findings of arthritis on other joints of the body were compared to the ADC values of the 41 patients who lacked arthritis, and no significant difference was found statistically (Table 5). ADC values of 21 patients who had clinical findings of enthesitis were compared to the ADC values of the 41 patients who did not have enthesitis, and no correlation was found statistically (Table 6). 4. Discussion Diagnosing sacroiliitis in patients with SpA is important in planning the treatment and for follow-up protocols [3,4]. Therefore, early diagnosis of sacroiliitis is crucial to prevent the possible complications in the late period of the disease [5]. However, clinical evaluation is limited; imaging is needed in most of the cases [6]. Although radiographs are easily available initial imaging method, there is a relatively long period between the occurrence of the symptoms and appearance of the findings on the radiographs. Moreover, the oblique course of the sacroiliac joint, the superposition of the sacral and iliac bones and wavy nature of the joint make the interpretation harder [6–8]. MRI can show the ligamentous and synovial components far better than any of the imaging methods and can depict the erosive or sclerotic changes, pathologies of the capsule and synovium, chondral lesions and marrow diseases [9]. There are some studies emphasizing on the use of contrast media in increasing the sensitivity of MRI for diagnosing activation of the disease [10]. Ability of MRI in showing active inflammation is
also another advantage as it is an important criterion in treatment planning. Therefore, MRI findings take place in the new diagnostic criteria of SpA according to ASAS, which has the highest sensitivity among all diagnostic criteria since June 2009 [1]. Although routine MRI has high sensitivity in showing the abovementioned abnormalities related to the sacroiliac joints and the bone marrow, these findings are mostly nonspecific. DWI-MRI has the potential of increasing the specificity of MRI [11]. The ADC value, a diffusivity index, is a quantitative marker for tissue characterization. The contribution of T2-weighting to DWI may cause false positive results as diffusion restriction, therefore qualitative assessment may not be efficient, and quantitative measurements should be made. There are some studies on differentiating benign and pathologic vertebra fractures by DWI and ADC measurements, which revealed lower ADC values for pathologic fractures [12,13]. However, despite quantitative measurements, DWI-MRI has its own limitations. For example, although it is mostly successful in differentiating benign and malignant fractures, there is significant overlap of ADC values in some cases. Differentiating treatment response from residual spinal metastases is mostly reliable but limited use is reported for evaluation of sclerotic bone metastases. Overlapping spectrum of DWI-MRI findings are also found for bone and soft tissue tumors and bone infection, limiting its clinical value [14]. We performed MRI and DWI in 62 patients with SpA and 40 subjects in the control group. The mean ADC values of the subchondral bone on both sacral and iliac joints are found as 0.23 × 10−3 mm2 /sn. Vertebral marrow has 20–70% fat component, which has low diffusivity, resulting in low ADC values. In other studies, vertebral ADC values were found ranging between 0.15 × 10−3 mm2 /sn and 0.59 × 10−3 mm2 /sn [15–17]. These low values are due to the slow diffusion of water molecules bounded to the fat molecules of the yellow marrow. Dietrich et al. [18] performed DWI with b value of 50 and 500 sn/mm2 , and found mean ADC value of 0.3 × 10−3 mm2 /sn, whereas Chan et al. [15] performed DWI at b value of only 1000 sn/mm2 , and reported the mean
Table 3 The ADC values of the patient and control groups on the right iliac bone. Right iliac ADC
Patient (n = 62)Mean ± SD
Control (n = 40)Mean ± SD
p
Superior Middle Inferior
0.47 × 10- 3 ± 0.19 0.48 × 10- 3 ± 0.18 0.54 × 10- 3 ± 0.22
0.20 × 10- 3 ± 0.07 0.24 × 10- 3 ± 0.09 0.26 × 10- 3 ± 0.09
<0.001 <0.001 <0.001
Table 4 The ADC values of the patient and control groups on the left iliac bone. Left iliac ADC
Patient (n = 62)Mean ± SD
Control (n = 40)Mean ± SD
p
Superior Middle Inferior
0.45 × 10- 3 ± 0.18 0.47 × 10- 3 ± 0.18 0.49 × 10- 3 ± 0.28
0.19 × 10- 3 ± 0.06 0.23 × 10- 3 ± 0.09 0.24 × 10- 3 ± 0.08
<0.001 <0.001 <0.001
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Table 5 The comparison of the ADC values of patients who had arthritis and who did not have arthritis. ADC
Arthritis (−) (n = 41)Mean ± SD
Arthritis (+) (n = 21)Mean ± SD
p
R Sacral Superior R Sacral Middle R Sacral Inferior R Iliac Superior R Iliac Middle R Iliac Inferior L Sacral Superior L Sacral Middle L Sacral Inferior L Iliac Superior L Iliac Middle L Iliac Inferior
0.44 × 10- 3 0.47 × 10- 3 0.52 × 10- 3 0.46 × 10- 3 0.46 × 10- 3 0.53 × 10- 3 0.45 × 10- 3 0.48 × 10- 3 0.49 × 10- 3 0.44 × 10- 3 0.48 × 10- 3 0.50 × 10- 3
0.47 × 10- 3 0.50 × 10- 3 0.48 × 10- 3 0.50 × 10- 3 0.50 × 10- 3 0.55 × 10- 3 0.44 × 10- 3 0.47 × 10- 3 0.51 × 10- 3 0.46 × 10- 3 0.46 × 10- 3 0.47 × 10- 3
0.341 0.693 0.120 0.587 0.672 0.994 0.624 0.246 0.760 0.818 0.225 0.301
± ± ± ± ± ± ± ± ± ± ± ±
0.11 0.12 0.15 0.12 0.12 0.21 0.14 0.18 0.13 0.16 0.13 0.17
± ± ± ± ± ± ± ± ± ± ± ±
0.10 0.16 0.10 0.29 0.26 0.25 0.12 0.24 0.13 0.22 0.26 0.20
Table 6 The comparison of the ADC values of patients who had enthesitis and who did not have enthesitis. ADC
Enthesitis (−) (n = 41)Mean ± SD
Enthesitis (+) (n = 21)Mean ± SD
p
R Sacral Superior R Sacral Middle R Sacral Inferior R Iliac Superior R Iliac Middle R Iliac Inferior L Sacral Superior L Sacral Middle L Sacral Inferior L Iliac Superior L Iliac Middle L Iliac Inferior
0.45 × 10- 3 0.50 × 10- 3 0.52 × 10- 3 0.49 × 10- 3 0.48 × 10- 3 0.57 × 10- 3 0.44 × 10- 3 0.49 × 10- 3 0.51 × 10- 3 0.46 × 10- 3 0.49 × 10- 3 0.51 × 10- 3
0.46 × 10- 3 0.44 × 10- 3 0.47 × 10- 3 0.44 × 10- 3 0.46 × 10- 3 0.46 × 10- 3 0.46 × 10- 3 0.43 × 10- 3 0.48 × 10- 3 0.43 × 10- 3 0.44 × 10- 3 0.46 × 10- 3
0.905 0.051 0.086 0.597 0.935 0.056 0.518 0.231 0.499 0.958 0.345 0.699
± ± ± ± ± ± ± ± ± ± ± ±
0.11 0.14 0.15 0.22 0.21 0.25 0.14 0.23 0.14 0.21 0.21 0.21
ADC value as 0.23 × 10−3 mm2 /sn. Bozgeyik et al. [19] obtained DWI at b values of 100, 600 and 1000 and calculated the mean ADC value as 0.67 × 10−3 mm2 /sn. The difference of ADC values in different studies was tributed to the different imaging techniques and b values. Age is also an important factor affecting the vertebral marrow component. By increasing age, osteoporotic changes may cause decrease in ADC values. The higher ADC values reported in the study of Bozgeyik et al. may be due to the younger study population (mean age 26). The mean ADC value of 0.86 × 10−3 mm2 /sn obtained from the hyperintense bone marrow areas is significantly higher than the control group. Moreover, the mean ADC value of 0.48 × 10−3 mm2 /sn obtained from the normal appearing subchondral areas adjacent to the sacroiliac joint is also significantly higher than the control group. This is thought to be due to the increase of the movement of the water molecules because of the bone marrow edema. Although there may not be signal alterations, quantitative measurements also show that there is increased diffusion in normal appearing areas. Therefore, in case of clinically diagnosed SpA, after excluding other pathologies both clinically and based on conventional MRI sequences, DWI images should be evaluated visually firstly, which may give the idea of increased diffusion in presence of high signal on ADC map. However, absence of signal alterations at first look should not deter the radiologist from the idea of possible sacroiliitis and therefore quantitative ADC measurements should be done. CRP and ESR are laboratory parameters of inflammation; there are some studies reporting that the increase in CRP and ESR may be used as a marker of inflammation and activity of the disease. In a study of Won-Hee Jee et al. [20], a correlation between ESR with CRP values and synovial contrast enhancement on MRI was reported. However, in a study by Puhakka et al. [2], there was no abnormality in the CRP values in patients who had sacroiliitis on MRI. To our knowledge, there is no other study searching any correlation between the ADC values and laboratory parameters. Although the number of patients is low, the findings in our study show that a
± ± ± ± ± ± ± ± ± ± ± ±
0.10 0.09 0.10 0.12 0.10 0.13 0.11 0.11 0.14 0.09 0.10 0.10
laboratory marker, CRP and an imaging marker, ADC may correlate well on the activity of the disease. The presence of clinical findings of SpA such as arthritis and enthesitis did not show any correlation with ADC values, however, the number of patients was not sufficient to make a statistical analysis. The reason of non-correlation may also be that most of the patients with arthritis and enthesitis were in the chronic stage of the disease. In conclusion, DWI is a sensitive, fast sequence which can help to differentiate normal and pathologic bone marrow areas by ADC measurements which cannot be visually evaluated. It can be used to diagnose early sacroiliitis in SpA patients and follow the treatment effects.
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Please cite this article in press as: Gezmis E, et al. Diagnosis of early sacroiliitis in seronegative spondyloarthropathies by DWI and correlation of clinical and laboratory findings with ADC values. Eur J Radiol (2013), http://dx.doi.org/10.1016/j.ejrad.2013.08.032