Graves' ophthalmopathy is a chronic autoimmune disease of the orbit and periorbital tissues. It usually affects both eyes but can be asymmetric and is more frequent in women.1,2 Approximately 20% of patients with Graves' disease have Graves' ophthalmopathy as the most common extrathyroidal manifestation.3 Although the pathogenesis of Graves' ophthalmopathy remains unclear, it is thought that autoantibodies target the thyrotropin receptor expressed by epithelial cells of the thyroid and orbital tissues.4
Within the orbit, the main manifestation is thickening of the extraocular muscles, which occurs through expansion of the connective tissue.5,6 Histologic features of the extraocular muscles in the early phase of Graves' ophthalmopathy are marked lymphocyte infiltration and interstitial edema, whereas in later stages fibrosis and fatty infiltration are seen.7 The most frequently affected muscles are the inferior and medial rectus.4
Orbital imaging plays an important role in the differential diagnosis and treatment of patients. Imaging is mandatory when there is asymmetric proptosis, active disease, and suspected optic neuropathy, and before decompression surgery.8 In patients with Graves' ophthalmopathy, the detection of enlarged extraocular muscles and excess orbital fat by magnetic resonance imaging (MRI)9 leads to its initial diagnosis, and this tool is also essential to monitor the course of Graves' ophthalmopathy. A major morphological diagnostic criterion is spindle-like spreading of the rectus muscle (> 4 mm) without tendon involvement.6,8 However, although MRI and computed tomography are currently the best imaging procedures for diagnosis of Graves' ophthalmopathy, computed tomography is limited due to radiation risks and MRI is not always easily available, resulting in appointment delays that may prevent an early diagnosis.6
More recently, optical coherence tomography (OCT) has been used to examine the anterior portion of the extraocular rectus muscles.10–20 Using OCT, Häner et al.18 were the first to describe medial rectus muscle thickening in 15 patients with Graves' ophthalmopathy. In a previous OCT study, we observed a thicker horizontal rectus muscle in patients with Graves' ophthalmopathy than in controls, and thicker measurements again in those with active Graves' ophthalmopathy disease.19 Further, in a pilot study, we were also able to detect by OCT extraocular muscle thinning in response to tocilizumab treatment in a series of five patients with Graves' ophthalmopathy.20
Despite these new tools available, no study has yet compared horizontal rectus muscle thickness measurements using OCT for the anterior portion and MRI for the muscle belly. The objective of the current study was therefore to assess correlations between these two imaging techniques for extraocular rectus muscle thickness measurements in patients with Graves' ophthalmopathy.
Patients and Methods
In this cross-sectional observational study, we examined 62 eyes of 31 patients with Graves' ophthalmopathy, 20 with inactive disease and 11 with cliniscally active Graves' ophthalmopathy, at the Hospital Clínico San Carlos, Madrid, Spain, from November 2016 to October 2017. The study protocol adhered to the tenets of the Declaration of Helsinki and was approved by the hospital review board. Signed informed consent was obtained from each participant. In all participants, we first performed an ophthalmologic examination and obtained complete medical records.
Active and inactive disease were defined according to the clinical activity score (CAS) of Mourits, in which 10 items are assessed to give a score out of 10: (1) chemosis; (2) caruncle inflammation; (3) conjunctival redness; (4) eyelid erythema; (5) eyelid swelling; (6) spontaneous orbital pain; (7) gaze-evoked orbital pain; (8) exophthalmos of 2 mm or greater; (9) impaired ocular motility; and (10) loss of visual acuity. The cut-off defining active disease was CAS 4/10 or greater.21
Patients were excluded if they had an ocular disease making it difficult to define the limbus (as the measurement reference point), were not able to easily collaborate, or had undergone strabismus surgery. Patients with clinically active Graves' ophthalmopathy were examined with both techniques (OCT and MRI) before starting treatment (both naïve or with a new active episode). The maximum acceptable interval between the two examinations was 3 months.
Further data collected for all participants were gender, age, thyroid state, Graves' ophthalmopathy disease duration, and CAS.
MRI examinations were performed in a 1.5 Tesla General Electric HDxt MRI scanner (GE Medical Systems, Milwaukee, WI) using paired surface coils and the following sequences were obtained: (1) axial T1-weighted spin echo images (field of view, slice thickness, and space between slices: 140, 2, and 0.5 mm, respectively); (2) axial fat-suppressed fast spin-echo (FSE) T2-weighted images (120, 3, and 1 mm, respectively); (3) coronal inversion recovery inferior rectus images (160, 3, and 1 mm, respectively); (4) coronal T1-weighted images (140, 2, and 0.5 mm, respectively); and (5) sagittal T2-weighted images (120, 3, and 1 mm, respectively). Coronal sequences were acquired on a plane perpendicular to the optic nerve and patients were asked to look forward. MRI scans were assessed by an experienced radiologist blinded to the clinical examinations. After excluding any other cause of orbital disease other than Graves' ophthalmopathy, extra-ocular muscle measurements were obtained. Although thicknesses of all extraocular muscles were measured, only medial rectus and lateral rectus measurements were considered in this study. Three measurements of the two muscles were made: maximum axial transversal diameter (T-MRI), maximum coronal or craniocaudal diameter (CC-MRI), and area (A-MRI). The measurements for T-MRI and CC-MRI were made on axial or coronal T1-weighted images and muscle areas were calculated in an AGFA Advanced 4.2 postprocess work station (Agfa HealthCare, Mortsel, Belgium).
The presence or absence of exophthalmos on the MRI was determined by drawing a line at the anterior portion of the zygomatic arches: exophthalmos was recorded when more than two-thirds of the ocular globe was anterior to this line.
Images were obtained using the anterior segment module of the Spectralis device (Heidelberg Engineering, Inc., Heidelberg, Germany). This system takes 40,000 axial scans per second and has a 7-µm axial resolution. Scans were performed parallel to the long axis of the muscle as five parallel line scans 16 mm long and 5.7 mm high at 278-µm intervals, and the best quality image selected. Cross-section photographs were obtained selecting the software's sclera mode. In addition, within this mode, we selected the line raster scanning protocol, enhanced depth imaging, and high resolution. Examination was guided with a fixation light: patients were asked to assume a maximal temporal gaze during medial rectus muscle scanning and a maximal nasal gaze for lateral rectus muscle scanning.12,13,19,20
Horizontal rectus muscle thicknesses were measured using the OCT's calliper function. The posterior limbus was readily identified as the point of reference for the measurements. Medial rectus muscle thickness was measured at 7.2 and 9.2 mm from the limbus (designated medial rectus [7.2] and me-dial rectus [9.2], and the lateral rectus at 8.5 mm from the limbus (lateral rectus [8.5]) (Figure 1). Scanning was performed by a well-trained examiner and all scans analyzed by a single well-trained image interpreter (LD-P-G-L).12,13,19,20
Medial rectus muscle thickness measurements by optical coherence tomography (OCT) and magnetic resonance imaging (MRI) in a patient with active phase Graves' ophthalmopathy (GO). (A) Medial rectus thickness measured at 7.2 and 9.2 mm from the limbus by OCT. (B) Maximum axial transversal diameter (T-MRI) and muscle area (A-MRI) measured by MRI in the axial view. (C) Maximum coronal or craniocaudal diameter (CC-MRI) measured in the coronal view.
Statistical tests were performed using SPSS software (Statistical Package for Social Sciences, version 18.0; SPSS, Inc., Chicago, IL). Quantitative data are provided as the mean and standard deviation, and qualitative data as their frequency distributions. The Spearman test was used to correlate the muscle measurements obtained by OCT and MRI, and also to detect correlations between intra-OCT or intra-MRI measurements. Significance was set at a P value of less than .05.
The study included 62 eyes of 31 patients with Graves' ophthalmopathy, 20 with inactive and 11 with clinically active disease. Mean age was 54.8 ± 12.7 years (range: 32 to 81 years) and 84% were women. Mean disease duration was 48.8 ± 51.3 months (range: 3 to 210 months). Mean CAS scores were 0.8 ± 0.9 (range: 0 to 3) in the inactive Graves' ophthalmopathy group and 4.8 ± 1.5 (range: 4 to 8) in the active Graves' ophthalmopathy group. Eighty-five percent of patients had hyperthyroidism. The remaining 15% were euthyroid. Exophthalmos was observed by MRI in 8 of 11 active patients with Graves' ophthalmopathy, and in 7 of 20 patients with inactive Graves' ophthalmopathy.
OCT medial rectus muscle thickness measurements for the inactive and active Graves' ophthalmopathy groups, respectively, were: 201.7 ± 47.5 and 204.9 ± 37.5 µm for medial rectus [7.2]; 239.9 ± 57.2 and 265.2 ± 74.3 µm for medial rectus [9.2]; and 232.6 ± 65.9 and 260.8 ± 75.6 µm for lateral rectus [8.5]. Differences between the two groups were not significant for both medial rectus and lateral rectus muscles (P ≥ .187) (Table 1).
Muscle Thickness Measurements in Patients With Inactive and Active Graves' Ophthalmopathy
According to our MRI medial rectus muscle thickness measurements, differences emerged between patients with inactive and active Graves' ophthalmopathy for all three measurement sites (T-MRI: 4.8 ± 1.5 vs 6.3 ± 1.9 mm, P = .004; CC-MRI: 10.1 ± 1.5 vs 11.2 ± 1.4 mm, P = .011; and A-MRI: 101.1 ± 42.5 vs 123.2 ± 37.2 mm, P < .001). Among the MRI measurements of lateral rectus thickness, a difference between patients with inactive and active Graves' ophthalmopathy was observed for A-MRI (84.9 ± 27.2 vs 101.3 ± 15.6 mm; P = .002) but not T-MRI or CC-MRI (P ≥ .170) (Table 1).
For the whole cohort, correlations of OCT measurements with MRI measurements (medial rectus [7.2] and medial rectus [9.2], respectively) were: T-MRI (R = 0.428 and 0.576, respectively; P ≤ .002), A-MRI (R = 0.562 and 0.674, respectively; P < .001), and CC-MRI (R = 0.286 and 0.293, respectively; P ≤ .046) (Table 2).
Results of the OCT and MRI Correlation Study
Nevertheless, these correlations were always higher in the patients with clinically active compared to inactive Graves' ophthalmopathy (for medial rectus [7.2] and medial rectus [9.2], respectively): OCT versus T-MRI (R = 0.604 and 0.576, respectively; P ≤ .010), OCT versus A-MRI (R = 0.678 and 0.706; P < .001), and OCT versus CC-MRI (R = 0.503; P = .028; and R = 0.256; P = .291) (Table 2).
In contrast, no correlations were observed between any of the OCT and MRI lateral rectus muscle thickness measurements (P ≥ .177) (Table 2).
Correlation between both medial rectus OCT measurements (medial rectus [7.2] and medial rectus [9.2]) was moderate for the whole Graves' ophthalmopathy patient series (R = 0.591; P < .001) and good for the inactive Graves' ophthalmopathy group (R = 0.756; P < .001) (Table 3). For the different MRI measurements, correlation between T-MRI and A-MRI was moderate for the whole Graves' ophthalmopathy group (R = 0.583; P < .001) but excellent in the subgroup of patients with active Graves' ophthalmopathy (R = 0.845; P < .001). In contrast, correlation between CC-MRI and T-MRI or A-MRI was weak (R ≤ 0.300; P ≥ .121).
Correlation Between Different Parameters Measured by the Same Technique
The most meaningful classic morphological sign found in Graves' ophthalmopathy is extraocular muscle enlargement. Many studies have shown the capacity of MRI to detect this.4,6,8 Interestingly, it is possible to measure horizontal rectus muscle enlargement in patients with Graves' ophthalmopathy by OCT because this method allows visualization of its anterior portion.18–20
In an OCT study, Häner et al.18 examined lateral rectus and medial rectus muscle thicknesses in 15 patients with Graves' ophthalmopathy, 5 of whom had active disease. These authors observed a mean thickness of the medial rectus muscle in the Graves' ophthalmopathy group of 256.4 ± 17 µm, significantly thicker than in their control group (214.7 ± 5.5 µm). In a previous study, we found that the horizontal rectus muscles were thicker in patients with Graves' ophthalmopathy than in controls and also in patients with clinically active Graves' ophthalmopathy compared to those with inactive disease.19 In the current study, patients with clinically active Graves' ophthalmopathy had thicker medial rectus and lateral rectus muscles than patients with inactive disease (239.9 ± 57.2 and 232.6 ± 65.9 µm vs 265.2 ± 74.3 and 260.8 ± 75.6 µm, respectively). However, these differences were not significant, perhaps because of our small sample size.
Using MRI in our Graves' ophthalmopathy population, we observed a thicker medial rectus muscle at all measurement sites in patients with Graves' ophthalmopathy with clinically active rather than inactive disease. The lateral rectus muscle area (A-MRI) was thicker, but no differences were noted in T-MRI or CC-MRI. In the patients with clinically active Graves' ophthalmopathy, mean medial rectus and lateral rectus thicknesses of 11.2 ± 1.4 and 10.0 ± 1.0 mm were observed, respectively, in the CC-MRI view. Similarly, Xu et al.22 reported vertical thicknesses in the coronal view for the medial rectus and lateral rectus muscles of 11.2 ± 2.4 and 10.4 ± 1.3 mm, respectively, in 33 patients with active Graves' ophthalmopathy. Both our study and their study identified a greater thickness of the medial rectus muscle, as classically described.
In the current correlation study between MRI and OCT, we were able to detect a significant moderate correlation in medial rectus muscle thickness measurements in patients with Graves' ophthalmopathy; this correlation was good in those with clinically active disease. The best correlation was observed between OCT-measured medial rectus muscle thickness and MRI-measured medial rectus muscle area in patients with both inactive and active Graves' ophthalmopathy. This could be because muscle area reflects the dimensions of the whole muscle (length and thickness), and not only a muscle section.
The second best correlation between OCT and MRI medial rectus muscle measurements was for T-MRI, which was higher than for CC-MRI for the whole Graves' ophthalmopathy cohort. This could be because A-MRI and T-MRI are measured in the same axial view and therefore correlate better with each other than with CC-MRI, which is measured in the coronal view.
We hypothesize that the better OCT-MRI correlations observed in patients with active rather than inactive disease may be attributed to thickening of the muscle allowing for better OCT visualization of the muscle edges, possibly making this measurement more accurate. Moreover, correlations between MRI parameters were stronger in the patients with active disease (A-MRI – T-MRI: R = 0.845 for active Graves' ophthalmopathy versus R = 0.491 for inactive Graves' ophthalmopathy).
Unlike for the medial rectus muscle, there was no correlation between OCT and MRI lateral rectus muscle thickness measurements in patients with inactive or active Graves' ophthalmopathy. Consistently, it is well known that the medial rectus muscle is usually more affected in patients with Graves' ophthalmopathy and the tendon is shorter. In prior work, we measured by OCT the distance from the limbus to the muscle insertions to be 5.2 mm for the medial rectus and 6.5 mm for the lateral rectus.12 To these distances, we would need to add the mean lengths of the tendons: approximately 4 mm for the medial rectus muscle and 8 mm for the lateral rectus muscle.23 According to these mean values, the true muscles begin approximately 9 mm from the limbus for the medial rectus muscle and 14 to 15 mm for the lateral rectus muscle. Thus, because the current furthest thickness measurements were made at 9.2 mm from the limbus for the medial rectus muscle and at 8.5 mm for the lateral rectus muscle, we assumed we were measuring the initial portion of the medial rectus muscle. However, for the lateral rectus muscle, we are probably measuring the thickness of the muscle or tendon rather than the muscle itself.
Unlike the situation with Graves' ophthalmopathy, idiopathic inflammation of the muscles or myositis also tends to involve the tendon.24 Nevertheless, tendon involvement does not preclude the possibility of diagnosing Graves' ophthalmopathy. Ben Simon et al.25 observed 6.4% of tendon involvement on computed tomography or MRI images. So it is not unreasonable to assume that in cases with more muscle fibers in the proximal tendon, we could see some tendon thickening associated with extraocular muscle enlargement related to Graves' ophthalmopathy. In a prior OCT study, we observed slight muscle enlargement in the anterior portion only (15 to 40 µm).19 This observation cannot be made by MRI because of the low resolution of the muscle insertion. Theoretically, because of its greater image resolution, OCT should enable clear distinction between muscle and tendon. However, it is still difficult to confirm real tendon involvement in Graves' ophthalmopathy.
According to our experience, OCT is able to detect neither the activity state of Graves' ophthalmopathy based on reflectivity nor the cause of muscle thickening because this occurs due to edema in active disease and fibrosis in inactive disease. In contrast, muscle inflammatory activity in patients with Graves' ophthalmopathy can be detected through MRI when a high signal intensity is observed in inversion recovery or short tau inversion recovery sequences.26,27 Mayer et al.26 and Tortora et al.27 reported good linear correlation between MRI sequence muscle brightness and the clinical features of inflammation in Graves' ophthalmopathy (quantified by CAS). However, Tortora et al.27 observed by MRI that there was no correlation between muscle diameters and CAS, confirming that muscle thickness alone is not a measure of the extent of inflammation. Accordingly, we observed thin muscles in patients with active disease (minimum values for medial rectus and lateral rectus of 134 and 127 µm, respectively) and thick muscles in patients with inactive disease (maximum values for medial rectus and lateral rectus of 407 and 363 µm, respectively).
It is unquestionable that MRI is currently the most effective tool for an initial diagnosis of Graves' ophthalmopathy and for monitoring its progression. MRI also allows visualization of both orbits simultaneously and the entire rectus muscles, including vertical muscles and their position within the orbit.6,8 Nevertheless, MRI has the drawbacks of being expensive, time-consuming, and claustrophobic, and of not usually being immediately available for use in routine clinical practice.
In contrast, OCT is a rapid non-invasive technique that may be performed at patient follow-up visits after an initial diagnosis of Graves' ophthalmopathy. However, this imaging procedure only serves to visualize the anterior portion and not the belly of the muscle.10–20 Accordingly, we suggest the possible use in daily practice of OCT as a rapid screening technique, mainly in cases of dubious diagnosis or during follow-up to determine whether there is thickening of the horizontal rectus muscles. Notwithstanding, we lack absolute OCT measurements indicating muscle enlargement that could diagnose the inflammatory state of Graves' ophthalmopathy.
Although Nianiaris et al.28 assessed the correlation between MRI and CT in Graves' ophthalmopathy, this is the first study to examine OCT-MRI muscle thickness measurement correlations in these patients. We recommend OCT as a complementary technique to MRI, which still should be considered the gold standard.
Our study has several limitations. The first and most important was that a correlation study was performed because an agreement study between OCT and MRI measurements at the same level of the muscle is not possible. The vertical rectus muscles are difficult to visualize by OCT because of interference by the eyelids and motility restrictions.11,12 Another limitation of this retrospective study was that MRI and OCT were not performed on the same day. Also, the gaze position, and therefore the muscle position during the exploration, was different between the two imaging techniques. In a healthy population study in 200 patients, Lerdlum et al.29 used computed tomography and observed that muscle thickness was linearly correlated with the angle of deviation for all rectus muscle thicknesses, being greater when the eye is in the direction of the muscle (relaxation). In our study, we analyzed muscle thickness by MRI in the primary position and by OCT in maximal lateral gaze. A further limitation of our study was the relatively low number of patients with active Graves' ophthalmopathy.
As improvements on our work to be considered in future prospective studies, we recommend assessment of the inferior rectus muscle in patients with Graves' ophthalmopathy using both OCT and MRI because this is the most affected extraocular muscle. Both imaging procedures should be conducted on the same day and in the same lateral gaze position to compare OCT with MRI findings. A more accurate method could also be to measure extraocular muscle volumes instead of diameters by MRI.30
OCT and MRI showed moderate significant correlation for medial rectus muscle thickness measurements in patients with Graves' ophthalmopathy. This correlation improved in those with clinically active disease. Accordingly, we propose OCT could be a good complementary imaging technique to MRI as a rapid screening tool for an early diagnosis in patients with Graves' ophthalmopathy to assess thickening of the anterior portion of the medial rectus or when MRI is not available.
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Muscle Thickness Measurements in Patients With Inactive and Active Graves' Ophthalmopathy
|MR OCT (mm)||[7.2]||201.7 ± 47.5 (138 to 305)||204.9 ± 37.5 (134 to 299)||.795|
|[9.2]||239.9 ± 57.2 (155 to 407)||265.2 ± 74.3 (140 to 414)||.187|
|LR OCT (mm)||[8.5]||232.6 ± 65.9 (118 to 363)||260.8 ± 75.6 (127 to 443)||.250|
|MR MRI (mm)|
|T-MRI||4.8 ± 1.5 (3.0 to 9.1)||6.3 ± 1.9 (4.1 to 10.0)||.004|
|CC-MRI||10.1 ± 1.5 (7.2 to 13.1)||11.2 ± 1.4 (9.0 to 13.2)||.011|
|A-MRI||101.1 ± 42.5 (49 to 194)||123.2 ± 37.2 (67 to 190)||< .001|
|LR MRI (mm)|
|T-MRI||4.2 ± 1.2 (2.1 to 6.9)||4.5 ± 1.0 (2.9 to 7.1)||.392|
|CC-MRI||9.8 ± 1.5 (6.0 to 12.1)||10.0 ± 1.0 (9.2 to 12.2)||.170|
|A-MRI||84.9 ± 27.2 (46 to 135)||101.3 ± 15.6 (70 to 133)||.002|
Results of the OCT and MRI Correlation Study
|Whole patient cohort|
| MR OCT|
| [7.2]||R = 0.428; P = .002||R = 0.286; P = .046||R = 0.562; P < .001|
| [9.2]||R = 0.576; P < .001||R = 0.293; P = .041||R = 0.674; P < .001|
| LR OCT|
| [8.5]||R = −0.087; P = .618||R = 0.059; P = .735||R = 0.241; P = .177|
| MR OCT|
| [7.2]||R = 0.439; P = .015||R = 0.162; P = .393||R = 0.570; P < .001|
| [9.2]||R = 0.544; P = .002||R = 0.156; P = .411||R = 0.634; P < .001|
| LR OCT|
| [8.5]||R = −0.168; P = .466||R = −0.021; P = .929||R = 0.097; P = .691|
| MR OCT|
| [7.2]||R = 0.604; P = .006||R = 0.503; P = .028||R = 0.678; P < .001|
| [9.2]||R = 0.576; P = .010||R = 0.256; P = .291||R = 0.706; P < .001|
| LR OCT|
| [8.5]||R = −0.080; P = .786||R = 0.116; P = .692||R = 0.251; P = .387|
Correlation Between Different Parameters Measured by the Same Technique
|Parameter||Total||Inactive GO||Active GO|
|OCT MR [7.2] – MR [9.2]||R = 0.591; P < .001||R = 0.756; P < .001||R = 0.471; P = .053|
|T-MRI – A-MRI||R = 0.583; P < .001||R = 0.491; P < .001||R = 0.845; P < .001|
|T-MRI – CC-MRI||R = 0.119; P = .416||R = 0.232; P = .217||R = −0.143; P = .559|
|A-MRI – CC-MRI||R = 0.167; P = .262||R = 0.300; P = .121||R = −0.116; P = .637|