Abstract
Objectives:
To accurately differentiate clumpy artifacts from tophi with foot and ankle DECT.
Methods and materials:
In session 1, 108 clumpy artifacts from 35 patients and 130 tophi images from 25 patients were analyzed. Reviewers classified green pixelation according to anatomic location, shape (linear, stippled, angular, oval), and height and width ratio. In session 2, green pixelation confined to the tendon was evaluated (shape, height and width ratio, occupied area in the tendon, accompanied peritendinous green pixelation).
Results:
In session 1, while tophi were noted at various locations, almost all clumpy artifacts were located at the tendon (99%, p < 0.0001). Most clumpy artifacts were linear, stippled, and wide, while most tophi were angular and oval (p < 0.05). In session 2, the shape of green pixelation from clumpy artifacts and tophi was significantly different (p < 0.0001) and most clumpy artifacts occupied less than 50% of the tendon (p = 0.02), and most tophi were accompanied by peritendinous green pixelation (p < 0.0001). Univariant logistic regression showed that tophi were significantly correlated with peritendinous deposits, angular and oval shape, and more than 50% of the tendon (p < 0.05).
Conclusion:
Clumpy artifacts can be differentiated from tophi in DECT. Clumpy artifacts typically are located in the tendon with a linear or stippled shape, wide, and less than 50% of a tendon’s cross-section. Tophi, on the other hand, typically are oval, larger than 50% of the tendon’s cross-section, and associated with adjacent peritendinous green pixelation.
Advances in knowledge:
Clumpy artifacts can be differentiated from tophi in image findings by their location and shape.
Introduction
Gout is caused by the deposition of monosodium urate (MSU) crystals in the joints. It causes swelling and pain and is the most common type of inflammatory arthropathy.1 For gout diagnosis, physicians rely on clinical presentation and elevated serum urate levels, with the gold standard being joint aspiration.2 However, joint aspiration is invasive and technically difficult, and has a false-negative rate of up to 25%3,4 and a false-positive rate of up to 24%.5
Dual-energy CT (DECT) can distinguish between urate and calcification using specific attenuation differences between two different voltage tube acquisitions.6–8 This has led to meaningful improvements in the diagnosis of gout over the last decade including (1) quantitative tophi volume analysis, (2) quantitative evaluation for treatment response, (3) diagnosis of subclinical MSU deposition, and (4) visualization of deep-sited tophi.9–12 As a consequence, DECT has been included in the 2015 gout classification criteria developed by the American College of Rheumatology and European League Against Rheumatism (ACR/EULAR) collaborative initiative.13
However, not all color-coded pixelation on DECT images is true urate deposition.14–17 Various types of artifacts have been reported, such as nail bed, skin, submillimeter, beam hardening, motion, vascular, and clumpy artifacts. Generally, these artifacts are unproblematic in everyday practice, as their characteristics are well established by previous reports.3,14–16,18,19 However, clumpy artifacts are problematic. We define “clumpy artifact”, following Jeon et al,15 who first coined the term, as a cluster of scattered submillimeter green pixelation. Various descriptions in previous studies of what we believe are the same phenomena include “tiny scattered green pixelations”, “diffuse pattern of the scattered submillimeter artifacts”, “cluster of submillimeter artifacts”, and, finally, “clumpy artifact”.14,15,20,21
Since clumpy artifacts usually appear as a concentrated cluster along a tendon or ligament, they resemble tophi in shape and location, which can frustrate diagnoses and lead to false-positives.15,22 Furthermore, a false-positive reading on DECT can easily lead to a false diagnosis under the ACR/EULAR classification criteria, since a positive imaging finding earns four points (and only eight points are required to make a diagnosis of gout).13 And a misinterpretation can lead to unnecessary gout treatment, which can result in adverse events such as Stevens-Johnson syndrome and bone marrow suppression. At the same time, patients receiving a misdiagnosis may miss their opportunity to get necessary and timely treatment of a genuine condition, including infection, a malignant mass, psoriasis, rheumatoid arthritis, calcium pyrophosphate deposition disease, or tenosynovial giant cell tumor (focal type).23
For these reasons, it is necessary to find a method to reliably differentiate clumpy artifact and tophi. However, to our knowledge, no study has focused on imaging findings of the clumpy artifact and how to differentiate them from tophi. Thus, the purpose of this study was to evaluate whether clumpy artifacts and tophi can be differentiated in foot and ankle DECT by comparing them in patients without and with gouty arthritis.
Methods and material
Patients
This retrospective study was approved by our institutional review board (Jeonbuk National University Hospital Institutional Review Board), and the requirement for written informed consent was waived. We retrospectively reviewed our institutional database for patients receiving foot and ankle DECT without a tin filter between February 2016 and July 2019. Green pixelation on DECT was observed in 138 of those patients. From those patients, we excluded patients who were under 16, had no 2D coronal multiplanar reformation (MPR) images or 3D Volume Rendering Technique (VRT) reconstruction images, had no clinical record describing symptoms available, or had a metal prosthesis, which resulted in a total of 94 patients. Using that cohort, we designed inclusion criteria for patients who definitively had gout and for patients who were extremely likely to be gout-free. The inclusion criteria for the gout group were as follows: they underwent CT for evaluation of gout, they visited a rheumatologist for foot pain, they had an ACR/EULAR classification criteria score over 8, and they showed high attenuation on standard gray-scale CT images obtained from DECT. In total, 130 green color coding (tophi) from 25 patients met these criteria for the gout group (joint aspiration performed in 2 out of 25 with positive MSU in polarised light microscopy). The inclusion criteria for the gout-free group were as follows: they underwent CT for reasons other than gout (such as trauma, osteochondral lesion, osteoarthritis, infection, and coalition), they had no history of gout or urate-lowering therapy, they had no high attenuation corresponding to green color on DECT, they had an ACR/EULAR classification criteria score under 8, they had no gout related code according to the ICD-10 (M10, M1A), they had no clinical symptoms suspected to be gout by a rheumatologist (time to maximal pain <24 h, resolution of symptoms in <14 days, or complete resolution between symptomatic episode), and, if measured, their uric acid was under 6 mg dl−1. In total, 108 green color coding (clumpy artifact) from 35 patients met these criteria for the gout-free group (Figure 1).
Figure 1.
Flowchart of the study population.
Image Acquisition
The images were obtained with a CT scanner in dual-source 64-MDCT dual-energy mode without a tin filter (Somatom Definition DS, Siemens Healthineers). The parameters were as follows: beam collimation, 64 × 0.6 mm; gantry rotation time, 0.5 sec; section reconstruction thickness, 0.75 mm; and image reconstruction interval, 0.5 mm. Data were acquired at 80 and 140 kV simultaneously and were then processed on a multimodality workstation (Syngo Via, Siemens Healthineers) with software (Syngo Via VB 10B, Siemens Healthineers) that used a 2-material decomposition algorithm and minimal HU set as 150. The software color-coded monosodium urate as green, cortical bone as blue, and trabecular bone as pink. This is based on the resets of the used software Visibility and color presets based on HU parameters that can be changed for each setting. The images were then displayed in 2D coronal MPR and 3D VRT reconstructions. During post-processing performed after scanning, all the following well-known DECT artifacts were removed under supervision of a radiologist to make sure the remaining green color coding was either a clumpy artifact or tophi: (1) nail or nail bed, (2) skin, (3) vessel, (4) cortex, (5) beam hardening artifact, and (6) single submillimeter artifacts.
Image Analysis
The following three images were taken from DECT: (1) standard gray-scale CT images, (2) 2D DECT MPR images with color mapping, and (3) 3D VRT images with color mapping. They were retrospectively analyzed with a picture archiving and communication system (Maroview, Seoul, Korea) by two experienced MSK radiologists (E.H.P. and Y.S.S, both with 9 years experience in musculoskeletal imaging) in consensus. The images were randomly assigned to mix gout-free and gout patients. All readers were blinded to patient medical information, clinical data, and other imaging modality findings.
The present study was composed of two sessions. In session 1, the reviewers classified green pixelation according to four different anatomic structures: periarticular, ligament, tendon, or other. Next, the reviewers were asked to identify the shape: linear, stippled, angular (triangular, rectangular, irregular), or oval (Figure 2). Next, the reviewers were asked to measure height and width (this was not done for stippled shape, since they had no definite height or width). Green color pixelation whose height was less than width was classified as a wider-than-tall pattern. This was done by matching green color coding at 3D VRT images and 2D MPR images. In session 2, green pixelation confined to the tendon was evaluated. The reviewers were asked to check whether the area of green color coding occupied more or less than 50% of the tendon’s cross-section (perpendicular to the longitudinal axis of the tendon with the greatest amount of green color coding) and whether there was accompanied peritendinous green pixelation.
Figure 2.
The shape of green pixelation (a-d) Schematic of shapes of green pixelation (a) stippled, (b) linear, (c) angular, (d) oval. (e-h) Green pixelation from clumpy artifacts (e-f) stippled, (g) linear, (h) angular. (i-l) Green pixelation from tophi (i-k) angular (i: rectangular, j: irregular, k: irregular), (l) oval.
Statistical Analysis
Statistical analyses were performed using statistical software (SAS v.9.4; SAS Institute Inc., Cary, NC, USA). The location, shape, height and width ratio, occupied area, and accompanied peritendinous green pixelation of clumpy artifacts and tophi were compared using Fisher’s exact test. Univariant logistic regression analyses were conducted for green pixelation confined to the tendon to identify which factors were significantly associated with gout when there was green color coding in the tendon.
Results
Session 1. green pixelation for all locations
The anatomic structures represented by green pixelation were significantly different between clumpy artifacts and tophi (p < 0.0001). The majority of clumpy artifacts were noted at the tendon (n = 107/108, 99.1%), and only one was noted at a ligament (n = 1/108, 0.9%, p < 0.0001). On the other hand, tophi were noted at various anatomic locations (periarticular [62.3%], ligament [13.1%], tendon [20%], and other [4.6%, subcutaneous layer = 5, fascia = 1]) (Figure 3, Table 1). There was a significant difference in shape between clumpy artifacts and tophi (p < 0.0001). While clumpy artifacts were mostly linear or stippled in shape, tophi were mostly angular or oval (p < 0.05). With linear shapes, clumpy artifacts were significantly more common than tophi (66/108, 61.1% vs 9/130, 6.9%, respectively, p < 0.0001). With stippled shapes, clumpy artifacts were also significantly more common than tophi (20/108, 18.5% vs 5/130, 3.8%, respectively, p = 0.0002). On the other hand, angular or oval shapes were significantly higher in tophi compared to the clumpy artifact (angular shape: 78/130, 60% vs 21/108, 19.4%, p < 0.0001; oval shape: 38/130, 29.2% vs 1/108, 0.9%, p < 0.0001)(Table 1). The height/width ratio of clumpy artifacts was frequently less than 1 (93.2%, p < 0.0001), which is wider-than-tall. The height/width ratio of tophi frequently was greater than or equal to 1 (66.7%) (Table 2, Figure 4).
Figure 3.
The image finding of clumpy artifacts vs tophi (anatomic structure). Cases that might result in false positives. (a-c) Clumpy artifact from a 50-year-old male (gout-free patient). Linear green pixelation is noted near the talocalcaneal joint (arrow in a). Note that the green pixelation (arrow) is within the tendon (FHL tendon, arrowheads) (b). There is no high attenuation visible on the standard gray-scale CT image. (d-f) Tophi from a 51-year-old male (gout patient). There is green pixelation near the talocalcaneal joint (arrow). The green pixelation seems similar to (a). However, the shape is more angular (triangular) (d). Note that the green pixelation (arrows) is not within the linear tendon (FHL tendon, arrowheads) as it is in (a) but next to it (e). A faint but definitive high attenuated lesion in the peritendinous area (arrow) is visible on a coronal standard gray-scale image (f).
Table 1.
Imaging findings of clumpy artifacts vs tophi
| Clumpy artifact (n = 108) |
Tophi (n = 130) |
P-value | |
|---|---|---|---|
| Anatomic structure | <0.0001 | ||
| periarticular | 0 (0.0) | 81 (62.3) | <0.0001 |
| ligament | 1 (0.9) | 17 (13.1) | 0.0004 |
| tendon | 107 (99.1) | 26 (20.0) | <0.0001 |
| others | 0 (0.0) | 6 (4.6) | 0.0237 |
| Shape | <0.0001 | ||
| linear | 66 (61.1) | 9 (6.9) | <0.0001 |
| stippled | 20 (18.5) | 5 (3.8) | 0.0002 |
| angular | 21 (19.4) | 78 (60.0) | <0.0001 |
| oval | 1 (0.9) | 38 (29.2) | <0.0001 |
Table 2.
Imaging findings of clumpy artifacts vs tophi
| Clumpy artifact (n = 88) |
Tophi (n = 126) |
P-value | |
|---|---|---|---|
| H/W ratio | <0.0001 | ||
| H/W ratio <1 | 82 (93.2) | 42 (33.3) | |
| H/W ratio ≥1 | 6 (6.8) | 84 (66.7) |
Figure 4.
The image findings of clumpy artifacts vs tophi. (a-b) Clumpy artifact in the tendon of FHL (which is known to have artifacts frequently) from a 61-year-old male (gout-free patient). The green color pixelation (arrow) is linear in shape, occupying less than 50% of the cross-section of the tendon (a). No matched high attenuation is noted at standard gray-scale CT images in the coronal plane (b) (c-d) Tophi in the tendon of FHL from a 70-year-old male (known gout patient). Although the location seems similar with (a), the green color coding (arrow) is oval in shape, occupying over 50% of the cross-section of the tendon (c). High attenuated tophi (arrows) are noted in a standard gray-scale image on the sagittal plane (d). (e-f) Tophi in the tendon of FHL from a 52-year-old male (known gout patient). Note that the green color coding is noted in FHL (arrow) and peritendinous area (arrowheads). Corresponding high attenuated tophi (arrow, arrowheads) in standard gray-scale CT image on the coronal plane (f).
Session 2. green pixelation confined to the tendon
The total number of clumpy artifacts and tophi enrolled in session 2 was 107 green pixelation areas from 35 gout-free patients (range = 1–12 number) and 26 green pixelation areas from 11 gout patients (range = 1–7 number), respectively. The shape of green pixelation confined to the tendon showed significant differences between clumpy artifacts and tophi (p < 0.0001). Linear shape was significantly frequent in clumpy artifacts compared with tophi (66/107, 61.7% vs 2/26, 7.7%, p < 0.0001). Although the difference did not reach statistical significance, stippled shape was more frequent in clumpy artifacts than tophi (20/107, 18.7% vs 2/26, 7.7%, p = 0.1758; Figures 4 and 5). Angular and oval shape were significantly frequent in tophi compared with clumpy artifacts (angular shape: 14/26, 53.8% vs 20/107, 18.7%, p = 0.0002; oval shape: 8/26, 30.8% vs 1/107, 0.9%, p < 0.0001)(Table 3).
Figure 5.
Comparison of green pixelation confined to the tendon (a-c) Tophi, shown as green pixelation in the tibialis anterior tendon, are dense showing an angular and oval shape (arrows in a,b) with accompanied peritendinous tophi (arrowheads in b). High attenuation tophi are noted at standard gray-scale CT (c). (d-f) Although there is no peritendinous lesion, green pixelation in the peroneus tendon are dense with an oval and rectangular shape (arrows in d,e). There are high attenuation tophi along the peroneus tendon in standard gray-scale CT (f). (g-i) Compared with tophi from a-f, clumpy artifacts show stippled green pixelation along the tibialis posterior tendon (arrows in g,h). No matched high attenuation is noted at standard gray-scale CT images in the sagittal plane (i).
Table 3.
Green pixelation confined to the tendon; imaging findings of clumpy artifacts vs tophi
| Clumpy artifact (n = 107) |
Tophi (n = 26) |
p-value | |
|---|---|---|---|
| Shape | <0.0001 | ||
| linear | 66 (61.7) | 2 (7.7) | <0.0001 |
| stippled | 20 (18.7) | 2 (7.7) | 0.1758 |
| angular | 20 (18.7) | 14 (53.8) | 0.0002 |
| oval | 1 (0.9) | 8 (30.8) | <0.0001 |
| Occupied area of the tendon in the cross-section | 0.0279 | ||
| less than 50% | 82 (76.6) | 14 (53.8) | |
| over 50% | 25 (23.4) | 12 (46.2) | |
| Peritendinous green pixelation | <0.0001 | ||
| non-accompanied | 107 (100.0) | 10 (38.5) | |
| accompanied | 0 (0.0) | 16 (61.5) | |
Clumpy artifacts tended to occupy less than 50% of the cross-section of the tendon (82/107, 76.6%), but tophi occupied less than 50% of the cross-section of the tendon in only half of the cases (14/26, 53.8%) (Figure 4; Table 3). The presence of peritendinous green pixelation was significantly different between clumpy artifacts and tophi in the tendon. While 16 out of 26 (61.5%) showed adjacent peritendonous green pixelation for tophi, there was no peritendinous green pixelation around clumpy artifacts (p < 0.0001, Table 3, Figure 4).
For height/width ratio, more clumpy artifacts had a wider-than-tall pattern compared to tophi (81/87, 93.1% vs 6/24, 25%, p < 0.0001, Table 4).
Table 4.
Green pixelation confined to the tendon; imaging findings of clumpy artifacts vs tophi
| Clumpy artifact (n = 87) |
Tophi (n = 24) |
P-value | |
|---|---|---|---|
| H/W ratio | <0.0001 | ||
| H/W ratio <1 | 81 (93.1) | 6 (25.0) | |
| H/W ratio ≥1 | 6 (6.9) | 18 (75.0) |
Univariable logistic regression showed that tophi were significantly correlated with peritendinous deposit (OR = 339.7, p < 0.0001), oval shape (OR = 150.7, p < 0.0001), height/width ratio over 1 (OR = 35.7, p < 0.0001), angular shape (18.8, p < 0.0001), and over 50% of the cross-section of the tendon occupation (OR = 2.9, p = 0.02).
Discussion
Clumpy artifacts, first introduced by Jeon et al15 are currently thought to be induced by noise without adequate energy separation, causing significant spectral overlap. While clumpy artifacts can be mitigated in some ways, (for example, DECT with a selective photon shield [tin filter] or by changing the minimum HU parameter,15,22) it is difficult to fully remove them. The present study demonstrated that image findings of clumpy artifacts, including location, shape, and height/width ratio, are significantly different than those of tophi.
The specificity of DECT is reportedly very high, up to 100% in one early study8 ; however, the specificity demonstrated in recent studies is reportedly lower (79%–83%).3,24 The reasons for lower specificity may vary, and one of them may be a high incidence of artifacts. While well-established common artifacts are known to not interfere with diagnostic accuracy,14,20 Park et al reported in a recent study that in certain settings of DECT, the clumpy artifact frequently occured and it was misinterpreted as gout in 23–55% of cases.17 A false-positive reading of DECT has a high impact under the ACR/EULAR classification criteria. A positive finding on DECT earns four points (and only eight points are required to make a diagnosis of gout). Further, there are no gradations in the imaging arm to account for small versus large volumes of pixelation or the experience levels of radiologists, so even with a small volume of clumpy artifacts, false-positive diagnoses can occur.22 So the most significant point of the present study is that, by being aware of image findings of clumpy artifacts, radiologists can make more precise diagnoses.
Glazebrook et al3 suggested that a greater clumped area of green pixelation within tendons may be the result of subclinical MSU deposition, and Mallinson et al14 suggested multiple tiny green foci in anatomical structures, such as along the tendons, true uric acid should be considered. However, in our study, clumpy artifacts were overwhelmingly noted at tendons. In total, 107 out of 108 clumpy artifacts were located at tendons. This result is in line with Jeon et al, who defined green pixelation on DECT along the tendon as artifacts by confirming negative findings with additional ultrasonography.15 This may be explained by the electron density of tendons. Artifacts of the heel pad and nail are explained by their increased CT number.3 The tendon is composed of densely packed collagen, elastin glycoprotein, and glycosaminoglycan,25,26 which is known to have a higher density on CT, measuring from 75 to 115 HU compared with muscle (55–60 HU) or fat (<0 HU).27 While clumpy artifacts were primarily located in the tendon, tophi were located in various structures including tendon, ligament, periarticular area, fascia, and bone.
While oval shape was significantly more prevalent in tophi compared with clumpy artifacts, clumpy artifacts were more linear in shape. And because of this, wider-than-tall green pixelation was significantly more prevalent with clumpy artifacts than with tophi (93.2% vs 33.3%, respectively, p < 0.0001). Stippled shape was also significantly more prevalent with clumpy artifacts compared with tophi (18.5% vs 3.8%, respectively, p = 0.0002).
Although the majority of clumpy artifacts were observed at tendons, this does not show all green pixelation confined to the tendon should be considered as clumpy artifacts. Tophi is also known to deposit in the tendon frequently, most commonly in the Achilles tendon in feet,28–30 and the present study demonstrated 26 out of 130 (20%) tophi were located at the tendon. For this reason green pixelation at the tendon(session 2) maybe challenging, and the present study found that clumpy artifacts can be differentiated from tophi. In terms of shape, while linear-shaped green pixelation tended to be clumpy artifacts, oval-shaped green color-coding tended to be tophi. In the same way, the ratio and occupied portion within the tendon differed. If the pattern was wider-than-tall and occupied less than 50% of the cross-section of the tendon, it was likely to be a clumpy artifact, and if it was taller-than-wide or occupied over 50% of the cross-section of the tendon, it was likely to be tophi. Another important finding of the present study was that the presence of adjacent peritendinous deposition was only noted in tophi. This is thought to be due to the fact that microcrystal deposition begins initially from the external part of the tendon, such as in the articular cartilage.28,29 Also in our study, there was no gout patient with tophi only located in the tendon.
Our study had some limitations. First, this study is a retrospective study. Although we recruited consecutive patients who strictly satisfied the inclusion criteria, there is still the possibility of selection bias. Second, the number of total patients included in the study is relatively small. While there was only one case where a clumpy artifact was noted in a location other than the tendon, studies with larger patient populations could reveal a higher incidence. Third, the location of green pixelation was only evaluated based on CT. In general, CT has a limitation with soft-tissue contrast. Hence, delineation of anatomic locations may involve a limitation. However, readers carefully paid attention to every anatomic site with green color pixelation by matching standard gray-scale images, 2D MPR images, and 3D VRT images. Fourth, irregular shapes were included in the category of angular. This was to make categorization easy and practical for clinicians in everyday practice. Unless the green color coding was linear or oval, both green color coding with acute (triangular, rectangular) and obtuse (irregular) angles were classified as angular. Fifth, pathologic confirmation was not performed for all green pixelation. Pathological confirmation of every green color pixelation is not possible for both clinical and ethical reasons. In addition, uric acid was not evaluated in all gout patients because uric acid can be normal in acute gout attacks. Hence, we set strict inclusion and exclusion criteria to subdivide gout-free and gout patients. And since the clumpy artifact can also exist on DECT in gout patients, for evaluation of tophi, we only included green pixelation that showed high attenuation in standard gray-scale CT. Further cadaveric studies might help clarify these findings. Sixth, only ankle and foot DECT were included in the study. Research is needed to see if result of our study applies similarly to other body parts. Finally, we did not evaluate diagnostic performance by applying the findings of this study. Further evaluation of radiologists’ performance in blind tests is required.
Conclusion
Clumpy artifacts are green pixelation usually located at the tendon. They can be differentiated from tophi by their linear shape with stippled patterns and a wider-than-tall appearance. When there is green pixelation at the tendon, tophi tend to be oval in shape, larger than 50% in cross-sectional area, and accompanied by adjacent peritendinous green pixelation.
Footnotes
Acknowledgment: We thank Wade Martin of Emareye Medical Editing for his critical review of this manuscript.
We thank Hanny Park, In Young Park for their thoughtful assistant.
Funding: This paper was supported by the Fund of Biomedical Research Institute, Jeonbuk National University Hospital
Contributor Information
Dong Han Shin, Email: syasdhll@gmail.com.
You Seon Song, Email: yssongrad@gmail.com.
Yunjung Choi, Email: cyjim@jbnu.ac.kr.
Wan-Hee Yoo, Email: ywhim@jbnu.ac.kr.
Florian Kummel, Email: florian.kuemmel@siemens-healthineers.com.
Eun Hae Park, Email: mbgracie@gmail.com.
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