MAGNETIC RESONANCE IMAGING AND COMPUTED TOMOGRAPHY FOR THE DETECTION AND CHARACTERIZATION OF NONMETALLIC INTRAOCULAR FOREIGN BODIES ELAD MOISSEIEV, MD,*† DAVID LAST, PHD,‡ DAVID GOEZ, PHD,‡ ADIEL BARAK, MD,*† YAEL MARDOR, PHD†‡ Purpose: To perform a comprehensive comparative analysis of nonmetallic intraocular foreign bodies (IOFBs) using computed tomography (CT) and magnetic resonance imaging (MRI). Methods: An ex vivo model of porcine eyes was used to study IOFBs consisting of 10 different materials: plastic, eyeglass lens, bottle glass, windshield glass, porcelain, gravel stone, concrete, wood, thorn, and pencil graphite. The study included 30 eyes with IOFBs and 6 control eyes. Each eye was scanned by CT and MRI. Images were analyzed by threedimensional viewing software to determine distinguishing characteristics for each material. Results: Analysis of MRI and CT scans yielded distinguishing characteristics for each of the 10 materials, and this information was integrated into a clinical algorithm that enables their distinction. More materials were identified by MRI than by CT, and smaller IOFB size was associated with lower detectability. Review of CT and head-coil MRI scans by masked specialists yielded a 95% agreement rate and allowed detection of most IOFBs. Conclusion: Magnetic resonance imaging was superior to CT in IOFB detection. Using these modalities, a set of distinguishing characteristics was established for the identification of the 10 studied materials. We recommend MRI to be part of the evaluation of patients with a suspected IOFB, after CT to rule out metallic IOFBs. RETINA 35:82–94, 2015
O
cular trauma is a major cause for irreversible loss of vision,1 and it is the most common cause of blindness among youths and young adults.2 According to several large series of patients who had penetrating ocular trauma, intraocular foreign bodies (IOFBs) may be present in as many as 18% to 41% of these cases.3–6 The presence of an IOFB indicates a more severe ocular injury and has been shown to be associated with a worse visual prognosis.7
A detailed ocular examination including dilated fundus examination should be performed as soon as possible in patients with penetrating ocular trauma and suspected IOFB. However, such patients often present with additional ocular pathologies such as traumatic cataract, vitreous hemorrhage, retinal detachment, or hyphema. In such situations, the presence of IOFBs might make the identification of these pathologies on examination more difficult or even impossible. In some cases, an IOFB is suspected from the mechanism of injury, and in others, it is revealed by imaging.8,9 As many as 20% of patients with IOFB may initially present with no complaints of pain or visual loss.10 Most eyes with penetrating or perforating injuries undergo primary closure as an emergency procedure, and it is important to know beforehand whether an IOFB is present in such eyes, as well as its composition, size, and
From the *Department of Ophthalmology, Tel Aviv Medical Center, Tel Aviv, Israel; †Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel; and ‡The Advanced Technology Center, Sheba Medical Center, Tel-Hashomer, Israel. None of the authors have any financial/conflicting interests to disclose. Reprint requests: Elad Moisseiev, MD, Department of Ophthalmology, Tel Aviv Medical Center, 6 Weizmann street, Tel Aviv, Israel 64239; e-mail: [email protected]
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location.8,11 An IOFB discovered intraoperatively will be extracted during surgery. However, if an IOFB is missed and discovered only postoperatively, an additional procedure for its extraction is almost always warranted.12 Factors associated with a worse visual prognosis in eyes with IOFBs include lower visual acuity on initial ocular examination, presence of a large IOFB, IOFB location on the posterior segment, presence of retinal detachment or endophthalmitis, and a longer time between injury and surgery for IOFB removal.12,13 Ultrasonography is an imaging technique that can be used for the detection, localization, or size measurement of IOFBs, as well as the detection of accompanied ocular pathology.14,15 However, it has several significant limitations. Ultrasonography is time consuming, operator-dependent, unable to distinguish the composition of the IOFB, and requires the cooperation of a patient who may be in severe pain.16 Pressure is exerted on the globe during an ocular ultrasonography procedure, and this may be hazardous for a patient who had a penetrating or perforating ocular trauma.16 Computed tomography (CT) is superior to ultrasonography in IOFB detection,8 and is the current standard clinical imaging technique for IOFB detection.17–19 Most IOFBs are metallic, and constitute 60 to 80% of all IOFBs.8,12,13 Nonmetallic IOFBs are typically fragments of glass or stone, and may also include wood and plastic.8,9,12,13,20 Most studies on IOFBs focused on metallic IOFBs, because of their higher incidence, and included only imaging by CT.9,14,21 Review of the literature revealed that no study focused on the identification, type detection, or size measurement of nonmetallic IOFBs using CT and/or magnetic resonance imaging (MRI). The purpose of this study was to perform a comprehensive comparative CT and MRI analysis of nonmetallic IOFBs in ex vivo porcine eyes. Images were acquired using CT
and MRI and the imaging characteristics of common materials of nonmetallic IOFBs were determined to assess the feasibility, accuracy, specificity, and efficacy of applying these scans for the identification of nonmetallic IOFBs.
Methods Foreign Bodies Ten materials that are commonly encountered as nonmetallic IOFBs in penetrating and perforating eye injuries were chosen. These materials included plastic, eyeglass lens (made of plastic polymer allyl diglycol carbonate, also known as “Columbia Resin #39” [CR39]), bottle glass, windshield glass, porcelain (china), stone (gravel stone), concrete, wood, thorn, and pencil graphite. Three fragments were obtained from each material to simulate IOFBs of different sizes. For each material, fragments of maximum diameters 3.0 mm, 2.0 mm, and 1.0 mm were studied. Examples of the material fragments used as IOFBs are shown in Figure 1. The lengths of the fragments were measured using a caliper before their inclusion in the study. Volumes were measured by water displacement according to Archimedes rule and rounded off to the nearest 1 mL. Model Eyes The study included 36 fresh unpreserved porcine eyes. The eyes were examined to ensure they had no abnormalities or damage before their use in the study. Intraocular foreign bodies were inserted into 30 of these eyes (10 materials · 3 sizes of fragments for each material). The remaining 6 eyes served as controls with no IOFB. This model has been previously used in experimental studies of IOFBs.9,14
Fig. 1. Samples of the materials used to simulate IOFBs in this study. Materials presented include plastic (A), eyeglass lens (CR39) (B), bottle glass (C), windshield glass (D), porcelain (E), gravel stone (F), concrete (G), wood (H), thorn (I), and pencil graphite (J).
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Intraocular Foreign Body Insertion Each eye was assigned an IOFB of a particular material and fragment size. The fragments were inserted into the vitreal space through a small pars plana incision made using a number 11 blade. All eyes were prepared in a standardized fashion by a single ophthalmologist (E.M.). Each eye contained only one IOFB and was numbered and marked to avoid confusion, and only the performing ophthalmologist was unmasked to the contents of each eye.
Imaging All eyes were scanned by CT and MRI within 3 hours of preparation. Computed tomography scans were obtained by helical CT technology (Brilliance 64; Philips Medical Systems, Cleveland, OH), using the standard protocol that is used for orbital imaging and IOFB detection. This included axial slices of 0.67-mm thickness and 0.33-mm intervals. The scan was performed at 250 milliamperes per second, and the window settings were 33/350. Coronal sections were reconstructed from the axial sections. Magnetic resonance images were acquired using a 1.5 Tesla interventional MRI scanner (Optima 450w; General Electric, Fairfield, CT). For optimal sensitivity and resolution, the eyes were scanned using a human phased–array wrist coil. To obtain unique signatures for each type of IOFB, the eyes were scanned by 2 spin-echo sequences, T1-weighted MRI (T1-MRI) and T2-weighted MRI (T2-MRI), both providing relatively low sensitivity to susceptibility artifacts but with different sensitivity to tissue/water contrast, and a gradientecho sequence (GE-MRI) providing high sensitivity to susceptibility artifacts. T1-weighted MR images were acquired with the following parameters: 10- · 10-cm field of view (FOV), 1-mm slice thickness, 0-mm slice intervals, 13.63-millisecond repetition time (TR), 611millisecond echo time (TE), and a bandwidth (BW) of 15.63 kHz. T2-MR images were acquired with: 10- · 10-cm FOV, 1-mm slice thickness, 0-mm slice intervals, TE of 85 milliseconds, TR of 5,548 milliseconds, and BW of 20.83 kHz. Gradient-echo sequence images were acquired with 10- · 10-cm FOV, 1-mm slice thickness, 0-mm slice intervals, TE of 13 milliseconds, TR of 300 milliseconds, a flip angle of 15°, and BW of 15.63 kHz. The wrist coil MRI provides excellent image resolution, however, it is too small for a patient’s head and therefore not practical for scanning eyes with suspected IOFBs in the clinical scenario. To simulate the clinical conditions of a patient undergoing MRI for the detection of an IOFB, the eyes were also scanned using a human phased–array head coil, with 1,500
mL of saline simulating the load of water in an average adult head. Each eye underwent T1-MRI, T2-MRI, and GE-MRI. T1-MR images were acquired with 18- · 18-cm FOV, 3-mm slice thickness, 0-mm slice intervals, TE of 28 milliseconds, TR of 360 milliseconds, and BW of 15 kHz. T2-MR images were acquired with 18- · 18-cm FOV, 3-mm slice thickness, 0-mm slice intervals, TE of 99 milliseconds, TR of 1,168 milliseconds, and BW of 100 kHz. Gradientecho sequence images were acquired with 18- · 18-cm FOV, 3-mm slice thickness, 0-mm slice intervals, TE of 15 milliseconds, TR of 580 milliseconds, a flip angle of 22°, and BW of 39 kHz. Image Analysis Altogether, each eye underwent 7 different scans (CT, and MRI including T1-, T2-, and GE-MRI in both wrist and head coils). Each scan of each eye was reviewed and analyzed using a three-dimensional viewing software developed under MATLAB (version R2010a, The MathWorks, Inc, Natick, MA), by a single ophthalmologist (E.M.). Wherever an IOFB was identified, it was marked as a region of interest in the image. In cases where an artifact was present, it was also included in the region of interest. For each IOFB and each scan type, the region of interest volumes were calculated. An example is shown in Figure 2. The calculated volumes were compared between the different scan types and compared with the volumes calculated using the water displacement method. The main outcome measure of this image analysis was to determine imaging characteristics for each of the studied materials. Secondary outcome measures included the proportion of IOFB identification with each modality and the effect of IOFB size on its detectability. Masked Image Review The images acquired using the CT and the head-coil MRI were separately and independently reviewed by three senior vitreoretinal surgeons, experienced in treating patients with IOFBs. These specialists were masked to the contents of the 36 eyes presented to them. For each scan, they were asked to indicate whether an IOFB was present in the eye or not. The main outcome measure of this analysis was correct identification of the presence of IOFBs in the eyes. Secondary outcome measure was the rate of agreement between the three specialists. Statistical Analysis Correlations between continuous variables were analyzed using Pearson’s correlation coefficient and
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Fig. 2. Top row: 6 sequential T1-MRI slices of an eye with a 2-mm gravestone IOFB. The IOFB is seen in the central 4 slices (the lens is seen in the first two). Bottom row: zoom into the region of the IOFB in the four slices in which it was seen. The borders of the IOFB were plotted in each image using the image analysis software (red dots), including any surrounding artifacts (such as the hyperintense ring around the void in this case). Intraocular foreign bodies volume was then calculated based on these regions of interest.
from the T1-, T2-, and GE-MR images and CT images were compared with the measured volumes of the 3-mm fragments before their insertion into the eyes (Table 1). In the MR images, the volumes of 7 of the materials were significantly increased, by a factor of at least 1.5, and the volumes of the remaining 3 materials (plastic, CR39 and wood) were slightly decreased. In the CT images, most IOFB volumes were slightly increased, three materials were hard to distinguish (plastic, CR39, and thorn), and one (wood) was undetectable. Similar volume trends were also demonstrated in the MR images and CT images of eyes with 2-mm and 1-mm IOFBs. Of note is the fact that all IOFBs were identifiable in the MR images, whereas 4 materials were undetectable in the CT for diameters less than 3 mm (plastic, CR39, wood, and thorn). Using the appearance of the IOFBs in T1-, T2-, and GE-MR images, their relative volumes in these images, and the appearance in CT images, a set of distinguishing characteristics has been established for
linear regression, and t-tests were used to analyze associations between categorical parameters. Data were analyzed using SPSS for Windows version 20 (SPSS Inc.; Chicago, IL). A P value of 0.05 was used to determine statistically significant differences between groups. Results Determination of Intraocular Foreign Body Material Characteristics The best sensitivity and image resolution was obtained by MRI using the wrist coil. All IOFBs of all sizes were clearly detected using this scanning technique. Magnetic resonance imaging was found superior to CT in demonstrating IOFBs of all materials. To determine unique characteristics for the identification of each of the 10 IOFB materials included in this study, information from the wrist coil MRI and the CT of eyes with 3-mm IOFBs was used. The calculated volumes
Table 1. Relationships Between Real IOFB Volumes and Their Calculated Volumes From T1-, T2-, GE-MRI Scans and CT Scans Material
T1/Real Volumes
T2/Real Volumes
GE/Real Volumes
CT/Real Volumes
Plastic CR39 (glasses) Glass (bottle) Windshield glass Porcelain Gravel stone Concrete Wood Thorn Graphite (pencil)
0.73 0.76 2.86 4.86 1.59 1.83 2.40 0.47 1.78 8.26
0.87 0.63 3.67 4.24 1.41 1.86 1.93 0.65 2.24 5.11
0.88 0.98 3.43 14.50 5.49 2.61 5.87 0.98 2.32 24.30
0.2 0.2 1.13 2.6 1.4 1.93 0.86 NA 0.53 1.14
NA, not available. The ratios provided reveal the magnification factor of each material by each scan (a value of 1.00 means equivalence to the volume measured using the water displacement method, ,1.00 means minification and .1.00 means magnification). The larger the value, the larger the material appears in the images and is easier to detect.
Plastic
CR39 (glasses)
Glass (bottle)
Void
Void
Void
T2 Appearance Void
Void
Void
GE Appearance Void
Void
Void
CT Appearance Barely detectable
Mildly hyperintense signal Hyperintense signal
T1/T2 Volumes 0.82
1.18
0.77
GE/T1 GE/T2 Volumes Volumes 1.22
1.20
1.19
Identifying Characteristics
1.01
Void in T1, T2, GE
1.50
Similar in size in T1, T2, GE Barely detectable on CT Void in T1, T2, GE
0.93
Slightly enlarged on GE Mildly hyperdense on CT Void in T1, T2, GE
Windshield glass
Distorted artifact, hypodense, and hyperdense elements
Distorted artifact, hypodense, and hyperdense elements
Void, surrounding hyperdense ring (scant)
Hyperintense signal
1.16
2.94
3.42
Porcelain
Void, surrounding hyperdense ring
Void, surrounding hyperdense ring
Void, surrounding hyperdense ring (scant)
Hyperintense signal
1.12
3.44
3.87
Gravel stone
Void, surrounding hyperdense ring
Void, surrounding hyperdense ring
Void
Hyperintense signal
0.98
1.42
1.40
Concrete
Void, surrounding hyperdense ring
Void, surrounding hyperdense ring
Void
Hyperintense signal
1.24
2.44
3.04
Similar in size in T1, T2, GE Bright hyperdensity on CT Distorted artifact, hypodensity and, hyperdensity on T1 and T2 Significantly enlarged on GE Scant hyperdense ring on CT Void with surrounding hyperdense ring on T1 and T2 hyperdense ring on GE Much larger on GE Void with surrounding hyperdense ring on T1 and T2 Void on GE Similar in size in T1, T2, GE Void with surrounding hyperdense ring on T1 and T2 Void on GE Much larger on GE
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T1 Appearance
Material
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Table 2. For Each Material, a Description of Its Appearance in T1-, T2-, GE-MRI and CT Scans is Provided, Along With Volume Ratios Between the MRI Sequences and a Summary of Its Unique Distinguishing Characteristics
Table 2. T1 Appearance
T2 Appearance
GE Appearance
CT Appearance
T1/T2 Volumes
GE/T1 GE/T2 Volumes Volumes
Wood
White halo (scant)
White halo
Void
Undetectable
1.08
2.10
2.28
Thorn
White halo
White halo
Void
Hypointense signal
0.79
1.30
1.03
Graphite (pencil)
Large distorted artifact, hypodense, and hyperdense elements
Large distorted artifact, hypodense, and hyperdense elements
Hyperintense Very large signal artifact, round, white halo (scant)
1.62
2.93
4.77
Identifying Characteristics Void with white halo on T1 and T2 Void on GE Larger on GE Undetectable on CT Void with white halo on T1 and T2 Void on GE Similar in size in T1, T2, GE Hypodense signal on CT Very large artifact on T1, T2, GE
Distortion with hyperdensity and hypodensity on T1 and T2 Significantly enlarged on GE Round artifact with scant white halo on GE
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Material
(Continued )
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Fig. 3. A graphic presentation of the distinguishing characteristics in MR and CT images of each of the 10 materials. For each material (A–J), 4 images are included, from left to right—T1-, T2-, and GE-MRI and CT. For each material, T1-, T2-, and GE-MR images of the same slice are presented. Noted are the distinguishing characteristics of each material: A. Plastic: void of similar size in T1-, T2-, and GE-MRI. Barely detectable by CT. B. CR39: void in T1-, T2-, and GE-MRI, volume slightly enlarged on GE-MRI. Mildly hyperintense signal on CT. C. Bottle glass: void of similar size in T1-, T2-, and GE-MRI. Bright hyperintense signal on CT. D. Windshield glass: distortion (note the “waves” around the IOFB) with hypodense and hyperdense elements on T1- and T2-MRI, significantly enlarged on GEMRI. Hyperintense signal on CT. E. Porcelain: void with surrounding ring of hyperdensity on T1- and T2-MRI. A scant ring is also noticed on GE-MRI, and the volume is enlarged. Hyperintense signal on CT. F. Gravel stone: void of similar size in T1-, T2-, and GE-MRI. A scant ring of hyperdensity is seen in T1- and T2- but not GE-MRI. Hyperintense signal on CT. G. Concrete: void with a scant ring of hyperdensity in T1- and T2-MRI. In GE-MRI, the ring is not seen and the volume is enlarged. Hyperintense signal on CT. H. Wood: a small signal with scant white halo on T1- and T2-MRI. The volume is significantly larger in GE-MRI. Undetectable by CT (no image). I. Thorn: a small signal with scant white halo on T1- and T2-MRI. The volume is similar in GE-MRI. Unique hypointense signal on CT. J. Pencil graphite: a large distorted artifact with hypodense and hyperdense elements on T1- and T2-MRI. Markedly enlarged on GE-MRI. The artifact is so large that it extends beyond the borders of the eye (in the third image [GE-MRI scan] the artifact is the covering part of an adjacent control eye). Hyperintense signal on CT.
MRI AND CT FOR NONMETALLIC IOFBs MOISSEIEV ET AL
the identification of each of the 10 materials. The unique imaging characteristics of each material are listed in Table 2, and examples of these characteristics for each material are shown in Figure 3. Effect of Intraocular Foreign Body Size on Identification Calculated volumes were generally larger in the MR images acquired using the head coil relative to those acquired with the wrist coil. The calculated volumes ratios between head and wrist coil images varied from 0.5 to 4.4. For quality control, correlations were studied between volume calculations based on T1-, T2-, and GE-MRI images for each IOFB size. Calculated volumes demonstrated significant correlation between MR images obtained by the wrist and the head coils (Table 3). Using the wrist coil MRI, all IOFB materials of all sizes were detectible in T1-, T2-, and GE-MR images. Using the head-coil MRI, sensitivity was lower and not all IOFBs could be detected. Calculated volumes of IOFBs scanned using the head coil were found to be larger than those scanned using the wrist coil. Smaller IOFBs sizes were harder to detect in the images acquired using the head coil and the increase in volume, relative to the wrist coil, was smaller. An example for the effect of IOFB size on its detection is shown in Figure 4. Smaller IOFB size also reduced its detectability by CT, because CT could detect only 9 of the 3-mm IOFBs, and only 6 of the 2-mm and 1-mm IOFBs. Masked Image Review Computed tomography and head-coil MR images were separately and independently reviewed by three senior vitreoretinal specialists. The scans were of 36 eyes (30 eyes with IOFBs of 10 materials and 3 sizes and 6 controls), and the specialists were asked to indicate whether an IOFB was present or not. Of 144 images (36 eyes, each with CT and T1-, T2-, and GEMR images acquired using the head coil) reviewed by Table 3. Correlations Between IOFBs Volumes Calculated From the MR Images Using the Wrist and the Head Coils MRI Scan T1 T2 GE
3-mm IOFBs
2-mm IOFBs
1-mm IOFBs
0.90 0.61 0.95
0.74 0.78 0.60
0.95 0.86 0.79
Correlations were calculated separately according to the scan type (T1-, T2-, and GE-MRI) and IOFB size. Values in the table refer to the r2 values of these correlations.
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each specialist, conflicting responses were found in only 6 scans. This represents a 95.83% rate of interobserver agreement. None of the specialists detected an IOFB in any of the control eyes. The results of the specialists’ analysis are presented in Table 4, and represent a simulation of the ability of each imaging modality to detect the various IOFB materials and sizes under realistic clinical circumstances. In the six cases where conflicting answers were given, the response agreed upon by two specialists was used. These results also demonstrated that smaller IOFB size reduced its detectability. In the CT images, the specialists identified 8 of the 3-mm IOFBs, and only 6 of the 2-mm and 1-mm IOFBs. In the T1-MR images, all 3-mm IOFBs were identified, decreasing to 7 of the 2-mm IOFBs and 6 of the 1-mm IOFBs. In the T2-MR images, 9 of the 3-mm IOFBs were identified, decreasing to 8 of the 2-mm IOFBs and 7 of the 1-mm IOFBs. In the GE-MR images, all 3-mm IOFBs were identified, decreasing to 8 of the 2-mm IOFBs and only 5 of the 1-mm IOFBs. Combining all 3 MRI types, the specialists detected all of the 3-mm IOFBs, 9 of the 2-mm IOFBs, and 8 of the 1-mm IOFBs.
Discussion The presence and composition of an IOFB may not be known at the presentation of patients with ocular trauma. These patients are often rushed to surgery for primary closure, and it is possible that an IOFB may be overlooked and remain in the eye even after surgery, causing additional damage, worsening the visual prognosis, and need for repeated intervention.12,13 Knowledge of the presence of an IOFB may change surgical strategy, and may help the surgeon decide on performing primary IOFB extraction, thus preventing additional surgery. Computed tomography is accepted as the imaging modality of choice in detecting and localizing metallic IOFBs,8,17–19,22–25 and may even serve in evaluating their size and composition.21 However, our review of the literature revealed no systematic evaluation of the assessment of nonmetallic IOFBs. A small recent study assessed ultrasonography for the detection of IOFBs and demonstrated that this imaging modality is able to detect nonmetallic IOFBs, but cannot differentiate between different materials, and in some cases, is also unable to differentiate between metallic and nonmetallic IOFBs.26 Although less frequent than metallic IOFBs,8,12,13 nonmetallic IOFBs are not rare in clinical practice and may be associated with significant ocular morbidity.27 Eyes with nonmetallic IOFBs may also have an unusual presentation, such as severe
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Fig. 4. The effect on IOFB size and its detectability by MR images acquired using a standard head coil. This example is of T1-MR images obtained using the wrist and head coils of eyes with CR39 IOFBs, demonstrating the reduced resolution of images obtained using the head coil. Presented are wrist and head-coil T1-MR images of eyes with CR39 IOFBs, at the sizes of 3 mm (A), 2 mm (B), and 1 mm (C). The 3-mm IOFB is clearly better demonstrated by the wrist coil images than the headcoil images. Calculated volumes were three times larger in the head-coil images (A). The 2-mm and 1-mm IOFB were demonstrated by the wrist coil images but undetectable in the head-coil images (B and C).
uveitis, and the diagnosis of the IOFBs may be considerably delayed.28 Our results indicate that MRI is superior to CT in the detection of nonmetallic IOFBs. Computed tomography is limited in detecting plastic, CR39, wood, and thorn IOFBs, whereas all materials were detected in the MR images. For any IOFB size, MR images detected more materials than CT. Using information by all 3 MRI scan types, almost all IOFBs could be detected (Table 4). Intraocular foreign bodies of all types were better demonstrated by MR images than CT, as can be seen from
the higher degree of magnification (ratio of the calculated volume from the images and from the water displacement method) obtained by MRI (Table 1). Magnetic resonance imaging offers a clear advantage over CT in the detection and localization of nonmetallic IOFBs, especially when their size is small. These results are consistent with an earlier study, using earlier versions of MRI and CT technologies, which also demonstrated better detectability of nonmetallic IOFBs with MRI.29 Analysis of MR images acquired using the wrist coil provided excellent resolution of the IOFB materials and
MRI AND CT FOR NONMETALLIC IOFBs MOISSEIEV ET AL Table 4. Detectability of the Various IOFB Materials and Sizes IOFB Material Plastic CR39 Glass (bottle) Windshield glass Porcelain Gravel stone Concrete Wood Thorn Graphite (pencil)
IOFB Size (mm)
CT
T1MRI
T2MRI
GEMRI
3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1
− − − + − − + + + + + + + + + + + + + + + − − − + − − + + +
+ + − + − − + + − + + + + + + + + − + + + + − − + − − + + +
+ + + + + + + + − + + + + + + + + + + + + − − − + − − + + +
+ + − + − − + + − + + + + + + + + + + + + + + − + − − + + +
Results are based on a masked image review of CT and headcoil MR images by three specialists. +, detected; −, undetected.
their identifying characteristics (Table 2 and Figure 3). The MR images acquired using the head coil were more representative of the clinical scenario of a real patient with ocular trauma. These images were lower in resolution and sensitivity compared with those obtained using the wrist coil. It is important to note that the significant correlation between MR images obtained by the wrist and the head coils (Table 3) indicates that operator-dependent measurement errors were not a cause for significant differences between volumes calculated for the same IOFB using different MRI coils. The reduced resolution of the head coil may explain the larger calculated volume measured from these scans, as well as the fact that some of the 2-mm and 1-mm IOFBs could not be detected by some of the scans (Figure 4). With reduced resolution, each pixel in the image represents a larger volume. For a given IOFB size, marking its artifact on a scan with lower resolution would therefore result in exaggerated size estimation. As IOFB decreases, it is possible that it would not be
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detectable anymore. The same material characteristics seen in wrist coil scans were seen in the head-coil scans, but the lower resolution caused their sizes to be somewhat enlarged when detected, and in some instances to be undetected by one of the scan types. Based on the information obtained from MRI and CT images, we were able to elucidate distinguishing features for all included IOFB materials. The 10 nonmetallic materials included as IOFBs in this study can be divided into 5 subgroups: 1. Plastic materials: This group includes plastic and CR39 from eyeglasses lenses. These substances appear as a void on T1-, T2-, and GE-MRI and are poorly detectable by CT. Columbia Resin #39 may be distinguished from plastic by its being enlarged approximately 50% on GE-MRI compared with T2-MRI. 2. Wood materials: This group contains wood and thorn. Both materials demonstrate a signal void surrounded by a white halo on T1- and T2-MRI, a signal void on GE-MRI, and are poorly detected by CT. They can be differentiated by the fact that wood is enlarged by nearly a factor of 2 on GE-MRI compared with T1- and T2-MRI, whereas thorn is not significantly enlarged. A unique hypointense signal was noted on CT for thorn, which was different from all other IOFBs, inducing a hyperintense signal. However, it was only seen with the 3-mm IOFB, and was undetected when its size was smaller. 3. Glass materials: This group includes bottle glass and car windshield glass. Bottle glass appears as a void on T1-, T2-, and GE-MRI, similarly to plastic substances. However, it is easily detected by CT and can therefore be easily distinguished from them. Windshield glass appears differently on MRI than bottle glass, inducing a large artifact with distortion, including hypointensity and hyperintensity elements in it, and demonstrating a significantly enlarged artifact on GE-MRI. It is possible that this appearance on MRI is due to traces of metal in the windshield glass fragments, because metal oxides are commonly used in windshields for deicing or heat-reflecting purposes. 4. Stone materials: This group includes gravel stone, concrete, and porcelain. All 3 materials appear as a void surrounded by a ring of hyperintensity on T1- and T2-MRI. They can be distinguished from each other by GE-MRI: gravel stone shows signal void and is not significantly enlarged, concrete shows signal void and is enlarged approximately by a factor of 3 compared with T1- and T2-MRI, and porcelain has a scant hyperintense ring and is
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Fig. 5. A flowchart for analysis of CT and MR imaging for distinguishing IOFB material composition. For simplicity, pencil graphite has been included in the stone materials group.
enlarged approximately by a factor of 3 compared with T1- and T2-MRI. 5. Pencil graphite: This material demonstrates a unique pattern on MRI, causing a large, distorted artifact, with hypointense and hyperintense elements. It appears much larger than it actually is on all MR images, with the artifact extending beyond the eyeball boundary, and is further enlarged on GE-MRI approximately 3 to 5 times more than on T1- and T2-MRI. This remarkable artifact is most probably due to the graphite diamagnetic properties, resulting in the induction of a magnetic field in opposition to an externally applied magnetic field. For this reason, the artifact is only seen on MRI (which involves an external magnetic field) and not on CT. These distinguishing features may be applied to the clinical scenario in the following manner: The first step in the preoperative assessment of patients with penetrating ocular trauma and suspected IOFB would be a CT scan, which will identify most metallic and some
nonmetallic IOFBs. If an IOFB is discovered, further imaging is not mandatory. Differentiating the IOFB composition is not obligatory, as it will be removed during surgery, and performing MRI on a patient with a metallic IOFB may be hazardous because the magnetic field might cause it to move and extend the ocular trauma.30–32 However, if an IOFB is not detected on CT, MRI should be obtained preoperatively, as it may reveal nonmetallic IOFBs missed by the CT. The higher resolution of the MR images may also detect minute metallic IOFBs that were missed by the CT. It has been demonstrated that small metallic IOFBs, undetectable by CT, are not displaced by the magnetic field forces of the MRI, and therefore performing MRI examinations in such cases is safe and will not cause additional damage.33–35 Additionally, if the mechanism of injury suggests a nonmetallic IOFB, MRI may be performed after detection of the IOFB by CT. We emphasize that any imaging should not be used to replace a detailed ocular examination in patients with ocular trauma, which should be performed as soon as possible.
MRI AND CT FOR NONMETALLIC IOFBs MOISSEIEV ET AL
The results of this study provide novel insights into the imaging of nonmetallic IOFBs, enabling clinicians to detect and identify nonmetallic IOFBs. This is the first study to establish a means of identifying and differentiating IOFB materials from their imaging characteristics. Additionally, it is the most comprehensive analysis of imaging nonmetallic IOFBs, including the detectability of various materials by CT and MRI and the effect of IOFB size on its detectability by them. Based on our results, in cases where no IOFBs are detected by CT, or the mechanism of injury suggests a nonmetallic IOFB, MR imaging should be performed as well. No individual scan type is sufficient for identifying IOFB material, but integration of information from various scan types makes proper identification of the materials possible. This valuable clinical tool is presented as a flowchart in Figure 5, which outlines the order in which the various imaging scans should be analyzed. Although most IOFBs were seen in CT as a nondistinct hyperintense signal (Figure 3), when this information is coupled with the IOFBs appearances on T1- and T2-MRI, it can lead clinicians to recognize the IOFB material type. When appearance on GE-MRI and other subtle characteristics are also considered, even IOFBs of similar material types can be clearly distinguished (Figure 5). To simulate the clinical utility of this study, 3 vitreoretinal specialists have reviewed the CT and head-coil MR images of all 36 eyes. The results of this masked image review were compatible with the unmasked analysis of the imaging data. Computed tomography is limited in detecting plastic, CR39, wood, and thorn IOFBs, whereas MRI is limited in detecting wood and thorn IOFBs (Table 4). This means that IOFBs comprised of wood material are most likely to be missed by imaging, especially in smaller sizes. The remaining materials are readily detectable by CT, MRI, or both, and their imaging characteristics may even serve in identifying their composition. This study provides the first comprehensive analysis of imaging by CT and MRI for the detection and identification of nonmetallic IOFBs. Our results demonstrate that MRI is superior to CT in detecting nonmetallic IOFBs. Moreover, the integration of information available from T1-, T2-, and GE-MRI and CT images may be used to identify the composition of such IOFBs. To the best of our knowledge, this is the first study to establish the distinguishing characteristics of nonmetallic materials that may complicate ocular injury as IOFBs, and enable their preoperative identification. These new findings have been translated into a clinical tool (Figure 5) that may serve clinicians in the identification of IOFB composition in patients with ocular trauma. Based on our results, we recommend that MR
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imaging should be considered in patients in whom a nonmetallic IOFB is suspected to be present and have a negative CT. Magnetic resonance imaging is able to detect more materials than CT, and at smaller sizes as well.12,29,36 According to our results, plastic and CR39 IOFBs are likely to be missed by CT and may be easily recognized by MRI. In addition, MRI may be valuable in cases where surgery has been performed to rule out a retained IOFB. It may enable clinicians to determine the composition of a nonmetallic IOFB, and aid in the consideration of repeated surgery. In conclusion, we have demonstrated that MRI is superior to CT in detecting nonmetallic IOFBs, and can also be used in conjunction with CT for the identification of their composition. We recommend MRI be considered in the evaluation of patients with a suspected IOFB and a negative CT, as well as in cases where the mechanism of injury suggest a nonmetallic IOFB. In the future, MRI may be more readily available in emergency situations, and the information detailed in this study may serve for accurate identification of presence and composition of nonmetallic IOFBs. Key words: intraocular foreign bodies, computed tomography, magnetic resonance imaging, nonmetallic. References 1. Negrel AD, Thylefors B. The global impact of eye injuries. Ophthalmic Epidemiol 1998;5:143–169. 2. Parver LM, Dannenberg AL, Blacklow B, et al. Characteristics and causes of penetrating eye injuries reported to the National Eye Trauma System Registry, 1985-91. Public Health Rep 1993;108:625–632. 3. De Juan E, Sternberg P, Michels RG. Penetrating ocular injuries: types of injuries and visual results. Ophthalmology 1983; 90:1318–1322. 4. Punnonen E, Laatikainen L. Prognosis of perforating eye injuries with intraocular foreign bodies. Acta Ophthalmol (Copenh) 1989;67:483–491. 5. Shock JP, Adams D. Long-term visual acuity results after penetrating and perforating ocular injuries. Am J Ophthalmol 1985;100:714–718. 6. Barak A, Elhalel A, Pikkel J, et al. Incidence and severity of ocular and adnexal injuries during the second Lebanon war among Israeli soldiers and civilians. Graefes Arch Clin Exp Ophthalmol 2011;249:1771–1774. 7. Yeh S, Colyer MH, Weichel ED. Current trends in the management of intraocular foreign bodies. Curr Opin Ophthalmol 2008;19:225–233. 8. Patel SN, Langer PD, Zarbin MA, Bhagat N. Diagnostic value of clinical examination and radiographic imaging in identification of intraocular foreign bodies in open globe injury. Eur J Ophthalmol 2012;22:259–268. 9. Gor DM, Kirsch CF, Leen J, et al. Radiologic differentiation of intraocular glass: evaluation of imaging techniques, glass types, size and effect of intraocular hemorrhage. AJR Am J Roentgenol 2001;177:1199–1203. 10. Kuhn F, Halda T, Witherspoon CD, et al. Intraocular foreign bodies: myths and truths. Eur J Ophthalmol 1996;6:464–471.
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11. Soheilian M, Feghi M, Yazdani S, et al. Surgical management of non-metallic and non-magnetic metallic intraocular foreign bodies. Ophthalmic Surg Lasers Imaging 2005;36: 189–196. 12. Zhang Y, Zhang M, Jiang C, Qiu HY. Intraocular foreign bodies in China: clinical characteristics, prognostic factors, and visual outcomes in 1421 eyes. Am J Ophthalmol 2011; 152:66–73. 13. Bai HQ, Yao L, Meng XX, et al. Visual outcome following intraocular foreign bodies: a retrospective review of 5-year clinical experience. Eur J Ophthalmol 2011;21:98–103. 14. Shiver SA, Lyon M, Blaivas M. Detection of metallic ocular foreign bodies with handheld sonography in a porcine model. J Ultrasound Med 2005;24:1341–1346. 15. Zhu Y, Zhang XF, Sheng YJ. Combining diagnosis of IOFB and complications with multiple image-related methods [in Chinese]. Zhonghua Yan Ke Za Zhi 2003;39:520–523. 16. Dunkin JM, Crum AV, Swanger RS, Bokhari SA. Globe trauma. Semin Ultrasound CT MR 2011;32:51–56. 17. Lakits A, Steiner E, Scholda C, et al. Evaluation of intraocular foreign bodies by spiral computed tomography and multiplanar reconstruction. Ophthalmology 1998;105:307–312. 18. Lakits A, Prokesch R, Scholda C, Bankier A. Orbital computed tomography in the diagnosis and management of eye trauma. Ophthalmology 1999;106:2330–2335. 19. Tonini M, Krainik A, Bessou P, et al. How helical CT helps the surgeon in oculo-orbital trauma. J Neuroradiol 2009;36: 185–198. 20. Lin HC, Wang HZ, Lai YH. Occult plastic intravitreal foreign body retained for 30 years: a case report. Kaohsiung J Med Sci 2006;22:529–533. 21. Briscoe D, Geffen N, Assia EI, Yaffe D. Determining size and characteristics of metal intraocular foreign bodies using helical CT scan. Eur J Ophthalmol 2009;19:861–865. 22. Maguire AM, Enger C, Eliott D, Zinreich SJ. Computed tomography in the evaluation of penetrating ocular injuries. Retina 1991;11:405–411. 23. Chacko JG, Figueroa RE, Johnson MH, et al. Detection and localization of steel intraocular foreign bodies using computed tomography. A comparison of helical and conventional axial scanning. Ophthalmology 1997;104:319–323.
24. Lakits A, Prokesch R, Scholda C, Bankier A. Multiplanar imaging in the preoperative assessment of metallic intraocular foreign bodies. Helical computed tomography versus conventional computed tomography. Ophthalmology 1998;105:1679–1685. 25. Papadopoulos A, Fotinos A, Maniatis V, et al. Assessment of intraocular foreign bodies by helical CT multiplanar imaging. Eur Radiol 2001;11:1502–1505. 26. Costa MA, Garcia PN, Barroso LF, et al. Composition of intraocular foreign bodies: experimental study of ultrasonographic presentation. Arq Bras Oftalmol 2013;76:13–17. 27. Olmos Zapata P, Güiote Torres A, Pérez Madera A. Epidemiological aspects of traumas with intraocular foreign bodies [in Spanish]. Arch Soc Esp Oftalmol 2005;80:19–25. 28. Sychev YV, Verner-Cole EA, Suhler EB, et al. Occult nonmetallic intraocular foreign bodies presenting as fulminant uveitis: a case series and review of the literature. Clin Ophthalmol 2013;7:1747–1751. 29. LoBue TD, Deutsch TA, Lobick J, Turner DA. Detection and localization of nonmetallic intraocular foreign bodies by magnetic resonance imaging. Arch Ophthalmol 1988;106:260–261. 30. Ta CN, Bowman RW. Hyphema caused by a metallic intraocular foreign body during magnetic resonance imaging. Am J Ophthalmol 2000;129:533–534. 31. Kremmer S, Schiefer U, Wilhelm H, Zrenner E. Mobilization of intraocular foreign bodies by magnetic resonance tomography [in German]. Klin Monbl Augenheilkd 1996;208:201–202. 32. Lagouros PA, Langer BG, Peyman GA, et al. Magnetic resonance imaging and intraocular foreign bodies. Arch Ophthalmol 1987;105:551–553. 33. Zhang Y, Cheng J, Bai J, et al. Tiny ferromagnetic intraocular foreign bodies detected by magnetic resonance imaging: a report of two cases. J Magn Reson Imaging 2009;29:704–707. 34. Williams S, Char DH, Dillon WP, et al. Ferrous intraocular foreign bodies and magnetic resonance imaging. Am J Ophthalmol 1988;105:398–401. 35. Williamson TH, Smith FW, Forrester JV. Magnetic resonance imaging of intraocular foreign bodies. Br J Ophthalmol 1989; 73:555–558. 36. Figueira EC, Francis IC, Wilcsek GA. Intraorbital glass foreign body missed on CT imaging. Ophthal Plast Reconstr Surg 2007; 23:80–82.
O
cular trauma is a major cause for irreversible loss of vision,1 and it is the most common cause of blindness among youths and young adults.2 According to several large series of patients who had penetrating ocular trauma, intraocular foreign bodies (IOFBs) may be present in as many as 18% to 41% of these cases.3–6 The presence of an IOFB indicates a more severe ocular injury and has been shown to be associated with a worse visual prognosis.7
A detailed ocular examination including dilated fundus examination should be performed as soon as possible in patients with penetrating ocular trauma and suspected IOFB. However, such patients often present with additional ocular pathologies such as traumatic cataract, vitreous hemorrhage, retinal detachment, or hyphema. In such situations, the presence of IOFBs might make the identification of these pathologies on examination more difficult or even impossible. In some cases, an IOFB is suspected from the mechanism of injury, and in others, it is revealed by imaging.8,9 As many as 20% of patients with IOFB may initially present with no complaints of pain or visual loss.10 Most eyes with penetrating or perforating injuries undergo primary closure as an emergency procedure, and it is important to know beforehand whether an IOFB is present in such eyes, as well as its composition, size, and
From the *Department of Ophthalmology, Tel Aviv Medical Center, Tel Aviv, Israel; †Sackler School of Medicine, Tel Aviv University, Tel Aviv, Israel; and ‡The Advanced Technology Center, Sheba Medical Center, Tel-Hashomer, Israel. None of the authors have any financial/conflicting interests to disclose. Reprint requests: Elad Moisseiev, MD, Department of Ophthalmology, Tel Aviv Medical Center, 6 Weizmann street, Tel Aviv, Israel 64239; e-mail: [email protected]
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location.8,11 An IOFB discovered intraoperatively will be extracted during surgery. However, if an IOFB is missed and discovered only postoperatively, an additional procedure for its extraction is almost always warranted.12 Factors associated with a worse visual prognosis in eyes with IOFBs include lower visual acuity on initial ocular examination, presence of a large IOFB, IOFB location on the posterior segment, presence of retinal detachment or endophthalmitis, and a longer time between injury and surgery for IOFB removal.12,13 Ultrasonography is an imaging technique that can be used for the detection, localization, or size measurement of IOFBs, as well as the detection of accompanied ocular pathology.14,15 However, it has several significant limitations. Ultrasonography is time consuming, operator-dependent, unable to distinguish the composition of the IOFB, and requires the cooperation of a patient who may be in severe pain.16 Pressure is exerted on the globe during an ocular ultrasonography procedure, and this may be hazardous for a patient who had a penetrating or perforating ocular trauma.16 Computed tomography (CT) is superior to ultrasonography in IOFB detection,8 and is the current standard clinical imaging technique for IOFB detection.17–19 Most IOFBs are metallic, and constitute 60 to 80% of all IOFBs.8,12,13 Nonmetallic IOFBs are typically fragments of glass or stone, and may also include wood and plastic.8,9,12,13,20 Most studies on IOFBs focused on metallic IOFBs, because of their higher incidence, and included only imaging by CT.9,14,21 Review of the literature revealed that no study focused on the identification, type detection, or size measurement of nonmetallic IOFBs using CT and/or magnetic resonance imaging (MRI). The purpose of this study was to perform a comprehensive comparative CT and MRI analysis of nonmetallic IOFBs in ex vivo porcine eyes. Images were acquired using CT
and MRI and the imaging characteristics of common materials of nonmetallic IOFBs were determined to assess the feasibility, accuracy, specificity, and efficacy of applying these scans for the identification of nonmetallic IOFBs.
Methods Foreign Bodies Ten materials that are commonly encountered as nonmetallic IOFBs in penetrating and perforating eye injuries were chosen. These materials included plastic, eyeglass lens (made of plastic polymer allyl diglycol carbonate, also known as “Columbia Resin #39” [CR39]), bottle glass, windshield glass, porcelain (china), stone (gravel stone), concrete, wood, thorn, and pencil graphite. Three fragments were obtained from each material to simulate IOFBs of different sizes. For each material, fragments of maximum diameters 3.0 mm, 2.0 mm, and 1.0 mm were studied. Examples of the material fragments used as IOFBs are shown in Figure 1. The lengths of the fragments were measured using a caliper before their inclusion in the study. Volumes were measured by water displacement according to Archimedes rule and rounded off to the nearest 1 mL. Model Eyes The study included 36 fresh unpreserved porcine eyes. The eyes were examined to ensure they had no abnormalities or damage before their use in the study. Intraocular foreign bodies were inserted into 30 of these eyes (10 materials · 3 sizes of fragments for each material). The remaining 6 eyes served as controls with no IOFB. This model has been previously used in experimental studies of IOFBs.9,14
Fig. 1. Samples of the materials used to simulate IOFBs in this study. Materials presented include plastic (A), eyeglass lens (CR39) (B), bottle glass (C), windshield glass (D), porcelain (E), gravel stone (F), concrete (G), wood (H), thorn (I), and pencil graphite (J).
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Intraocular Foreign Body Insertion Each eye was assigned an IOFB of a particular material and fragment size. The fragments were inserted into the vitreal space through a small pars plana incision made using a number 11 blade. All eyes were prepared in a standardized fashion by a single ophthalmologist (E.M.). Each eye contained only one IOFB and was numbered and marked to avoid confusion, and only the performing ophthalmologist was unmasked to the contents of each eye.
Imaging All eyes were scanned by CT and MRI within 3 hours of preparation. Computed tomography scans were obtained by helical CT technology (Brilliance 64; Philips Medical Systems, Cleveland, OH), using the standard protocol that is used for orbital imaging and IOFB detection. This included axial slices of 0.67-mm thickness and 0.33-mm intervals. The scan was performed at 250 milliamperes per second, and the window settings were 33/350. Coronal sections were reconstructed from the axial sections. Magnetic resonance images were acquired using a 1.5 Tesla interventional MRI scanner (Optima 450w; General Electric, Fairfield, CT). For optimal sensitivity and resolution, the eyes were scanned using a human phased–array wrist coil. To obtain unique signatures for each type of IOFB, the eyes were scanned by 2 spin-echo sequences, T1-weighted MRI (T1-MRI) and T2-weighted MRI (T2-MRI), both providing relatively low sensitivity to susceptibility artifacts but with different sensitivity to tissue/water contrast, and a gradientecho sequence (GE-MRI) providing high sensitivity to susceptibility artifacts. T1-weighted MR images were acquired with the following parameters: 10- · 10-cm field of view (FOV), 1-mm slice thickness, 0-mm slice intervals, 13.63-millisecond repetition time (TR), 611millisecond echo time (TE), and a bandwidth (BW) of 15.63 kHz. T2-MR images were acquired with: 10- · 10-cm FOV, 1-mm slice thickness, 0-mm slice intervals, TE of 85 milliseconds, TR of 5,548 milliseconds, and BW of 20.83 kHz. Gradient-echo sequence images were acquired with 10- · 10-cm FOV, 1-mm slice thickness, 0-mm slice intervals, TE of 13 milliseconds, TR of 300 milliseconds, a flip angle of 15°, and BW of 15.63 kHz. The wrist coil MRI provides excellent image resolution, however, it is too small for a patient’s head and therefore not practical for scanning eyes with suspected IOFBs in the clinical scenario. To simulate the clinical conditions of a patient undergoing MRI for the detection of an IOFB, the eyes were also scanned using a human phased–array head coil, with 1,500
mL of saline simulating the load of water in an average adult head. Each eye underwent T1-MRI, T2-MRI, and GE-MRI. T1-MR images were acquired with 18- · 18-cm FOV, 3-mm slice thickness, 0-mm slice intervals, TE of 28 milliseconds, TR of 360 milliseconds, and BW of 15 kHz. T2-MR images were acquired with 18- · 18-cm FOV, 3-mm slice thickness, 0-mm slice intervals, TE of 99 milliseconds, TR of 1,168 milliseconds, and BW of 100 kHz. Gradientecho sequence images were acquired with 18- · 18-cm FOV, 3-mm slice thickness, 0-mm slice intervals, TE of 15 milliseconds, TR of 580 milliseconds, a flip angle of 22°, and BW of 39 kHz. Image Analysis Altogether, each eye underwent 7 different scans (CT, and MRI including T1-, T2-, and GE-MRI in both wrist and head coils). Each scan of each eye was reviewed and analyzed using a three-dimensional viewing software developed under MATLAB (version R2010a, The MathWorks, Inc, Natick, MA), by a single ophthalmologist (E.M.). Wherever an IOFB was identified, it was marked as a region of interest in the image. In cases where an artifact was present, it was also included in the region of interest. For each IOFB and each scan type, the region of interest volumes were calculated. An example is shown in Figure 2. The calculated volumes were compared between the different scan types and compared with the volumes calculated using the water displacement method. The main outcome measure of this image analysis was to determine imaging characteristics for each of the studied materials. Secondary outcome measures included the proportion of IOFB identification with each modality and the effect of IOFB size on its detectability. Masked Image Review The images acquired using the CT and the head-coil MRI were separately and independently reviewed by three senior vitreoretinal surgeons, experienced in treating patients with IOFBs. These specialists were masked to the contents of the 36 eyes presented to them. For each scan, they were asked to indicate whether an IOFB was present in the eye or not. The main outcome measure of this analysis was correct identification of the presence of IOFBs in the eyes. Secondary outcome measure was the rate of agreement between the three specialists. Statistical Analysis Correlations between continuous variables were analyzed using Pearson’s correlation coefficient and
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Fig. 2. Top row: 6 sequential T1-MRI slices of an eye with a 2-mm gravestone IOFB. The IOFB is seen in the central 4 slices (the lens is seen in the first two). Bottom row: zoom into the region of the IOFB in the four slices in which it was seen. The borders of the IOFB were plotted in each image using the image analysis software (red dots), including any surrounding artifacts (such as the hyperintense ring around the void in this case). Intraocular foreign bodies volume was then calculated based on these regions of interest.
from the T1-, T2-, and GE-MR images and CT images were compared with the measured volumes of the 3-mm fragments before their insertion into the eyes (Table 1). In the MR images, the volumes of 7 of the materials were significantly increased, by a factor of at least 1.5, and the volumes of the remaining 3 materials (plastic, CR39 and wood) were slightly decreased. In the CT images, most IOFB volumes were slightly increased, three materials were hard to distinguish (plastic, CR39, and thorn), and one (wood) was undetectable. Similar volume trends were also demonstrated in the MR images and CT images of eyes with 2-mm and 1-mm IOFBs. Of note is the fact that all IOFBs were identifiable in the MR images, whereas 4 materials were undetectable in the CT for diameters less than 3 mm (plastic, CR39, wood, and thorn). Using the appearance of the IOFBs in T1-, T2-, and GE-MR images, their relative volumes in these images, and the appearance in CT images, a set of distinguishing characteristics has been established for
linear regression, and t-tests were used to analyze associations between categorical parameters. Data were analyzed using SPSS for Windows version 20 (SPSS Inc.; Chicago, IL). A P value of 0.05 was used to determine statistically significant differences between groups. Results Determination of Intraocular Foreign Body Material Characteristics The best sensitivity and image resolution was obtained by MRI using the wrist coil. All IOFBs of all sizes were clearly detected using this scanning technique. Magnetic resonance imaging was found superior to CT in demonstrating IOFBs of all materials. To determine unique characteristics for the identification of each of the 10 IOFB materials included in this study, information from the wrist coil MRI and the CT of eyes with 3-mm IOFBs was used. The calculated volumes
Table 1. Relationships Between Real IOFB Volumes and Their Calculated Volumes From T1-, T2-, GE-MRI Scans and CT Scans Material
T1/Real Volumes
T2/Real Volumes
GE/Real Volumes
CT/Real Volumes
Plastic CR39 (glasses) Glass (bottle) Windshield glass Porcelain Gravel stone Concrete Wood Thorn Graphite (pencil)
0.73 0.76 2.86 4.86 1.59 1.83 2.40 0.47 1.78 8.26
0.87 0.63 3.67 4.24 1.41 1.86 1.93 0.65 2.24 5.11
0.88 0.98 3.43 14.50 5.49 2.61 5.87 0.98 2.32 24.30
0.2 0.2 1.13 2.6 1.4 1.93 0.86 NA 0.53 1.14
NA, not available. The ratios provided reveal the magnification factor of each material by each scan (a value of 1.00 means equivalence to the volume measured using the water displacement method, ,1.00 means minification and .1.00 means magnification). The larger the value, the larger the material appears in the images and is easier to detect.
Plastic
CR39 (glasses)
Glass (bottle)
Void
Void
Void
T2 Appearance Void
Void
Void
GE Appearance Void
Void
Void
CT Appearance Barely detectable
Mildly hyperintense signal Hyperintense signal
T1/T2 Volumes 0.82
1.18
0.77
GE/T1 GE/T2 Volumes Volumes 1.22
1.20
1.19
Identifying Characteristics
1.01
Void in T1, T2, GE
1.50
Similar in size in T1, T2, GE Barely detectable on CT Void in T1, T2, GE
0.93
Slightly enlarged on GE Mildly hyperdense on CT Void in T1, T2, GE
Windshield glass
Distorted artifact, hypodense, and hyperdense elements
Distorted artifact, hypodense, and hyperdense elements
Void, surrounding hyperdense ring (scant)
Hyperintense signal
1.16
2.94
3.42
Porcelain
Void, surrounding hyperdense ring
Void, surrounding hyperdense ring
Void, surrounding hyperdense ring (scant)
Hyperintense signal
1.12
3.44
3.87
Gravel stone
Void, surrounding hyperdense ring
Void, surrounding hyperdense ring
Void
Hyperintense signal
0.98
1.42
1.40
Concrete
Void, surrounding hyperdense ring
Void, surrounding hyperdense ring
Void
Hyperintense signal
1.24
2.44
3.04
Similar in size in T1, T2, GE Bright hyperdensity on CT Distorted artifact, hypodensity and, hyperdensity on T1 and T2 Significantly enlarged on GE Scant hyperdense ring on CT Void with surrounding hyperdense ring on T1 and T2 hyperdense ring on GE Much larger on GE Void with surrounding hyperdense ring on T1 and T2 Void on GE Similar in size in T1, T2, GE Void with surrounding hyperdense ring on T1 and T2 Void on GE Much larger on GE
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T1 Appearance
Material
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Table 2. For Each Material, a Description of Its Appearance in T1-, T2-, GE-MRI and CT Scans is Provided, Along With Volume Ratios Between the MRI Sequences and a Summary of Its Unique Distinguishing Characteristics
Table 2. T1 Appearance
T2 Appearance
GE Appearance
CT Appearance
T1/T2 Volumes
GE/T1 GE/T2 Volumes Volumes
Wood
White halo (scant)
White halo
Void
Undetectable
1.08
2.10
2.28
Thorn
White halo
White halo
Void
Hypointense signal
0.79
1.30
1.03
Graphite (pencil)
Large distorted artifact, hypodense, and hyperdense elements
Large distorted artifact, hypodense, and hyperdense elements
Hyperintense Very large signal artifact, round, white halo (scant)
1.62
2.93
4.77
Identifying Characteristics Void with white halo on T1 and T2 Void on GE Larger on GE Undetectable on CT Void with white halo on T1 and T2 Void on GE Similar in size in T1, T2, GE Hypodense signal on CT Very large artifact on T1, T2, GE
Distortion with hyperdensity and hypodensity on T1 and T2 Significantly enlarged on GE Round artifact with scant white halo on GE
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Material
(Continued )
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Fig. 3. A graphic presentation of the distinguishing characteristics in MR and CT images of each of the 10 materials. For each material (A–J), 4 images are included, from left to right—T1-, T2-, and GE-MRI and CT. For each material, T1-, T2-, and GE-MR images of the same slice are presented. Noted are the distinguishing characteristics of each material: A. Plastic: void of similar size in T1-, T2-, and GE-MRI. Barely detectable by CT. B. CR39: void in T1-, T2-, and GE-MRI, volume slightly enlarged on GE-MRI. Mildly hyperintense signal on CT. C. Bottle glass: void of similar size in T1-, T2-, and GE-MRI. Bright hyperintense signal on CT. D. Windshield glass: distortion (note the “waves” around the IOFB) with hypodense and hyperdense elements on T1- and T2-MRI, significantly enlarged on GEMRI. Hyperintense signal on CT. E. Porcelain: void with surrounding ring of hyperdensity on T1- and T2-MRI. A scant ring is also noticed on GE-MRI, and the volume is enlarged. Hyperintense signal on CT. F. Gravel stone: void of similar size in T1-, T2-, and GE-MRI. A scant ring of hyperdensity is seen in T1- and T2- but not GE-MRI. Hyperintense signal on CT. G. Concrete: void with a scant ring of hyperdensity in T1- and T2-MRI. In GE-MRI, the ring is not seen and the volume is enlarged. Hyperintense signal on CT. H. Wood: a small signal with scant white halo on T1- and T2-MRI. The volume is significantly larger in GE-MRI. Undetectable by CT (no image). I. Thorn: a small signal with scant white halo on T1- and T2-MRI. The volume is similar in GE-MRI. Unique hypointense signal on CT. J. Pencil graphite: a large distorted artifact with hypodense and hyperdense elements on T1- and T2-MRI. Markedly enlarged on GE-MRI. The artifact is so large that it extends beyond the borders of the eye (in the third image [GE-MRI scan] the artifact is the covering part of an adjacent control eye). Hyperintense signal on CT.
MRI AND CT FOR NONMETALLIC IOFBs MOISSEIEV ET AL
the identification of each of the 10 materials. The unique imaging characteristics of each material are listed in Table 2, and examples of these characteristics for each material are shown in Figure 3. Effect of Intraocular Foreign Body Size on Identification Calculated volumes were generally larger in the MR images acquired using the head coil relative to those acquired with the wrist coil. The calculated volumes ratios between head and wrist coil images varied from 0.5 to 4.4. For quality control, correlations were studied between volume calculations based on T1-, T2-, and GE-MRI images for each IOFB size. Calculated volumes demonstrated significant correlation between MR images obtained by the wrist and the head coils (Table 3). Using the wrist coil MRI, all IOFB materials of all sizes were detectible in T1-, T2-, and GE-MR images. Using the head-coil MRI, sensitivity was lower and not all IOFBs could be detected. Calculated volumes of IOFBs scanned using the head coil were found to be larger than those scanned using the wrist coil. Smaller IOFBs sizes were harder to detect in the images acquired using the head coil and the increase in volume, relative to the wrist coil, was smaller. An example for the effect of IOFB size on its detection is shown in Figure 4. Smaller IOFB size also reduced its detectability by CT, because CT could detect only 9 of the 3-mm IOFBs, and only 6 of the 2-mm and 1-mm IOFBs. Masked Image Review Computed tomography and head-coil MR images were separately and independently reviewed by three senior vitreoretinal specialists. The scans were of 36 eyes (30 eyes with IOFBs of 10 materials and 3 sizes and 6 controls), and the specialists were asked to indicate whether an IOFB was present or not. Of 144 images (36 eyes, each with CT and T1-, T2-, and GEMR images acquired using the head coil) reviewed by Table 3. Correlations Between IOFBs Volumes Calculated From the MR Images Using the Wrist and the Head Coils MRI Scan T1 T2 GE
3-mm IOFBs
2-mm IOFBs
1-mm IOFBs
0.90 0.61 0.95
0.74 0.78 0.60
0.95 0.86 0.79
Correlations were calculated separately according to the scan type (T1-, T2-, and GE-MRI) and IOFB size. Values in the table refer to the r2 values of these correlations.
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each specialist, conflicting responses were found in only 6 scans. This represents a 95.83% rate of interobserver agreement. None of the specialists detected an IOFB in any of the control eyes. The results of the specialists’ analysis are presented in Table 4, and represent a simulation of the ability of each imaging modality to detect the various IOFB materials and sizes under realistic clinical circumstances. In the six cases where conflicting answers were given, the response agreed upon by two specialists was used. These results also demonstrated that smaller IOFB size reduced its detectability. In the CT images, the specialists identified 8 of the 3-mm IOFBs, and only 6 of the 2-mm and 1-mm IOFBs. In the T1-MR images, all 3-mm IOFBs were identified, decreasing to 7 of the 2-mm IOFBs and 6 of the 1-mm IOFBs. In the T2-MR images, 9 of the 3-mm IOFBs were identified, decreasing to 8 of the 2-mm IOFBs and 7 of the 1-mm IOFBs. In the GE-MR images, all 3-mm IOFBs were identified, decreasing to 8 of the 2-mm IOFBs and only 5 of the 1-mm IOFBs. Combining all 3 MRI types, the specialists detected all of the 3-mm IOFBs, 9 of the 2-mm IOFBs, and 8 of the 1-mm IOFBs.
Discussion The presence and composition of an IOFB may not be known at the presentation of patients with ocular trauma. These patients are often rushed to surgery for primary closure, and it is possible that an IOFB may be overlooked and remain in the eye even after surgery, causing additional damage, worsening the visual prognosis, and need for repeated intervention.12,13 Knowledge of the presence of an IOFB may change surgical strategy, and may help the surgeon decide on performing primary IOFB extraction, thus preventing additional surgery. Computed tomography is accepted as the imaging modality of choice in detecting and localizing metallic IOFBs,8,17–19,22–25 and may even serve in evaluating their size and composition.21 However, our review of the literature revealed no systematic evaluation of the assessment of nonmetallic IOFBs. A small recent study assessed ultrasonography for the detection of IOFBs and demonstrated that this imaging modality is able to detect nonmetallic IOFBs, but cannot differentiate between different materials, and in some cases, is also unable to differentiate between metallic and nonmetallic IOFBs.26 Although less frequent than metallic IOFBs,8,12,13 nonmetallic IOFBs are not rare in clinical practice and may be associated with significant ocular morbidity.27 Eyes with nonmetallic IOFBs may also have an unusual presentation, such as severe
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Fig. 4. The effect on IOFB size and its detectability by MR images acquired using a standard head coil. This example is of T1-MR images obtained using the wrist and head coils of eyes with CR39 IOFBs, demonstrating the reduced resolution of images obtained using the head coil. Presented are wrist and head-coil T1-MR images of eyes with CR39 IOFBs, at the sizes of 3 mm (A), 2 mm (B), and 1 mm (C). The 3-mm IOFB is clearly better demonstrated by the wrist coil images than the headcoil images. Calculated volumes were three times larger in the head-coil images (A). The 2-mm and 1-mm IOFB were demonstrated by the wrist coil images but undetectable in the head-coil images (B and C).
uveitis, and the diagnosis of the IOFBs may be considerably delayed.28 Our results indicate that MRI is superior to CT in the detection of nonmetallic IOFBs. Computed tomography is limited in detecting plastic, CR39, wood, and thorn IOFBs, whereas all materials were detected in the MR images. For any IOFB size, MR images detected more materials than CT. Using information by all 3 MRI scan types, almost all IOFBs could be detected (Table 4). Intraocular foreign bodies of all types were better demonstrated by MR images than CT, as can be seen from
the higher degree of magnification (ratio of the calculated volume from the images and from the water displacement method) obtained by MRI (Table 1). Magnetic resonance imaging offers a clear advantage over CT in the detection and localization of nonmetallic IOFBs, especially when their size is small. These results are consistent with an earlier study, using earlier versions of MRI and CT technologies, which also demonstrated better detectability of nonmetallic IOFBs with MRI.29 Analysis of MR images acquired using the wrist coil provided excellent resolution of the IOFB materials and
MRI AND CT FOR NONMETALLIC IOFBs MOISSEIEV ET AL Table 4. Detectability of the Various IOFB Materials and Sizes IOFB Material Plastic CR39 Glass (bottle) Windshield glass Porcelain Gravel stone Concrete Wood Thorn Graphite (pencil)
IOFB Size (mm)
CT
T1MRI
T2MRI
GEMRI
3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1 3 2 1
− − − + − − + + + + + + + + + + + + + + + − − − + − − + + +
+ + − + − − + + − + + + + + + + + − + + + + − − + − − + + +
+ + + + + + + + − + + + + + + + + + + + + − − − + − − + + +
+ + − + − − + + − + + + + + + + + + + + + + + − + − − + + +
Results are based on a masked image review of CT and headcoil MR images by three specialists. +, detected; −, undetected.
their identifying characteristics (Table 2 and Figure 3). The MR images acquired using the head coil were more representative of the clinical scenario of a real patient with ocular trauma. These images were lower in resolution and sensitivity compared with those obtained using the wrist coil. It is important to note that the significant correlation between MR images obtained by the wrist and the head coils (Table 3) indicates that operator-dependent measurement errors were not a cause for significant differences between volumes calculated for the same IOFB using different MRI coils. The reduced resolution of the head coil may explain the larger calculated volume measured from these scans, as well as the fact that some of the 2-mm and 1-mm IOFBs could not be detected by some of the scans (Figure 4). With reduced resolution, each pixel in the image represents a larger volume. For a given IOFB size, marking its artifact on a scan with lower resolution would therefore result in exaggerated size estimation. As IOFB decreases, it is possible that it would not be
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detectable anymore. The same material characteristics seen in wrist coil scans were seen in the head-coil scans, but the lower resolution caused their sizes to be somewhat enlarged when detected, and in some instances to be undetected by one of the scan types. Based on the information obtained from MRI and CT images, we were able to elucidate distinguishing features for all included IOFB materials. The 10 nonmetallic materials included as IOFBs in this study can be divided into 5 subgroups: 1. Plastic materials: This group includes plastic and CR39 from eyeglasses lenses. These substances appear as a void on T1-, T2-, and GE-MRI and are poorly detectable by CT. Columbia Resin #39 may be distinguished from plastic by its being enlarged approximately 50% on GE-MRI compared with T2-MRI. 2. Wood materials: This group contains wood and thorn. Both materials demonstrate a signal void surrounded by a white halo on T1- and T2-MRI, a signal void on GE-MRI, and are poorly detected by CT. They can be differentiated by the fact that wood is enlarged by nearly a factor of 2 on GE-MRI compared with T1- and T2-MRI, whereas thorn is not significantly enlarged. A unique hypointense signal was noted on CT for thorn, which was different from all other IOFBs, inducing a hyperintense signal. However, it was only seen with the 3-mm IOFB, and was undetected when its size was smaller. 3. Glass materials: This group includes bottle glass and car windshield glass. Bottle glass appears as a void on T1-, T2-, and GE-MRI, similarly to plastic substances. However, it is easily detected by CT and can therefore be easily distinguished from them. Windshield glass appears differently on MRI than bottle glass, inducing a large artifact with distortion, including hypointensity and hyperintensity elements in it, and demonstrating a significantly enlarged artifact on GE-MRI. It is possible that this appearance on MRI is due to traces of metal in the windshield glass fragments, because metal oxides are commonly used in windshields for deicing or heat-reflecting purposes. 4. Stone materials: This group includes gravel stone, concrete, and porcelain. All 3 materials appear as a void surrounded by a ring of hyperintensity on T1- and T2-MRI. They can be distinguished from each other by GE-MRI: gravel stone shows signal void and is not significantly enlarged, concrete shows signal void and is enlarged approximately by a factor of 3 compared with T1- and T2-MRI, and porcelain has a scant hyperintense ring and is
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Fig. 5. A flowchart for analysis of CT and MR imaging for distinguishing IOFB material composition. For simplicity, pencil graphite has been included in the stone materials group.
enlarged approximately by a factor of 3 compared with T1- and T2-MRI. 5. Pencil graphite: This material demonstrates a unique pattern on MRI, causing a large, distorted artifact, with hypointense and hyperintense elements. It appears much larger than it actually is on all MR images, with the artifact extending beyond the eyeball boundary, and is further enlarged on GE-MRI approximately 3 to 5 times more than on T1- and T2-MRI. This remarkable artifact is most probably due to the graphite diamagnetic properties, resulting in the induction of a magnetic field in opposition to an externally applied magnetic field. For this reason, the artifact is only seen on MRI (which involves an external magnetic field) and not on CT. These distinguishing features may be applied to the clinical scenario in the following manner: The first step in the preoperative assessment of patients with penetrating ocular trauma and suspected IOFB would be a CT scan, which will identify most metallic and some
nonmetallic IOFBs. If an IOFB is discovered, further imaging is not mandatory. Differentiating the IOFB composition is not obligatory, as it will be removed during surgery, and performing MRI on a patient with a metallic IOFB may be hazardous because the magnetic field might cause it to move and extend the ocular trauma.30–32 However, if an IOFB is not detected on CT, MRI should be obtained preoperatively, as it may reveal nonmetallic IOFBs missed by the CT. The higher resolution of the MR images may also detect minute metallic IOFBs that were missed by the CT. It has been demonstrated that small metallic IOFBs, undetectable by CT, are not displaced by the magnetic field forces of the MRI, and therefore performing MRI examinations in such cases is safe and will not cause additional damage.33–35 Additionally, if the mechanism of injury suggests a nonmetallic IOFB, MRI may be performed after detection of the IOFB by CT. We emphasize that any imaging should not be used to replace a detailed ocular examination in patients with ocular trauma, which should be performed as soon as possible.
MRI AND CT FOR NONMETALLIC IOFBs MOISSEIEV ET AL
The results of this study provide novel insights into the imaging of nonmetallic IOFBs, enabling clinicians to detect and identify nonmetallic IOFBs. This is the first study to establish a means of identifying and differentiating IOFB materials from their imaging characteristics. Additionally, it is the most comprehensive analysis of imaging nonmetallic IOFBs, including the detectability of various materials by CT and MRI and the effect of IOFB size on its detectability by them. Based on our results, in cases where no IOFBs are detected by CT, or the mechanism of injury suggests a nonmetallic IOFB, MR imaging should be performed as well. No individual scan type is sufficient for identifying IOFB material, but integration of information from various scan types makes proper identification of the materials possible. This valuable clinical tool is presented as a flowchart in Figure 5, which outlines the order in which the various imaging scans should be analyzed. Although most IOFBs were seen in CT as a nondistinct hyperintense signal (Figure 3), when this information is coupled with the IOFBs appearances on T1- and T2-MRI, it can lead clinicians to recognize the IOFB material type. When appearance on GE-MRI and other subtle characteristics are also considered, even IOFBs of similar material types can be clearly distinguished (Figure 5). To simulate the clinical utility of this study, 3 vitreoretinal specialists have reviewed the CT and head-coil MR images of all 36 eyes. The results of this masked image review were compatible with the unmasked analysis of the imaging data. Computed tomography is limited in detecting plastic, CR39, wood, and thorn IOFBs, whereas MRI is limited in detecting wood and thorn IOFBs (Table 4). This means that IOFBs comprised of wood material are most likely to be missed by imaging, especially in smaller sizes. The remaining materials are readily detectable by CT, MRI, or both, and their imaging characteristics may even serve in identifying their composition. This study provides the first comprehensive analysis of imaging by CT and MRI for the detection and identification of nonmetallic IOFBs. Our results demonstrate that MRI is superior to CT in detecting nonmetallic IOFBs. Moreover, the integration of information available from T1-, T2-, and GE-MRI and CT images may be used to identify the composition of such IOFBs. To the best of our knowledge, this is the first study to establish the distinguishing characteristics of nonmetallic materials that may complicate ocular injury as IOFBs, and enable their preoperative identification. These new findings have been translated into a clinical tool (Figure 5) that may serve clinicians in the identification of IOFB composition in patients with ocular trauma. Based on our results, we recommend that MR
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imaging should be considered in patients in whom a nonmetallic IOFB is suspected to be present and have a negative CT. Magnetic resonance imaging is able to detect more materials than CT, and at smaller sizes as well.12,29,36 According to our results, plastic and CR39 IOFBs are likely to be missed by CT and may be easily recognized by MRI. In addition, MRI may be valuable in cases where surgery has been performed to rule out a retained IOFB. It may enable clinicians to determine the composition of a nonmetallic IOFB, and aid in the consideration of repeated surgery. In conclusion, we have demonstrated that MRI is superior to CT in detecting nonmetallic IOFBs, and can also be used in conjunction with CT for the identification of their composition. We recommend MRI be considered in the evaluation of patients with a suspected IOFB and a negative CT, as well as in cases where the mechanism of injury suggest a nonmetallic IOFB. In the future, MRI may be more readily available in emergency situations, and the information detailed in this study may serve for accurate identification of presence and composition of nonmetallic IOFBs. Key words: intraocular foreign bodies, computed tomography, magnetic resonance imaging, nonmetallic. References 1. Negrel AD, Thylefors B. The global impact of eye injuries. Ophthalmic Epidemiol 1998;5:143–169. 2. Parver LM, Dannenberg AL, Blacklow B, et al. Characteristics and causes of penetrating eye injuries reported to the National Eye Trauma System Registry, 1985-91. Public Health Rep 1993;108:625–632. 3. De Juan E, Sternberg P, Michels RG. Penetrating ocular injuries: types of injuries and visual results. Ophthalmology 1983; 90:1318–1322. 4. Punnonen E, Laatikainen L. Prognosis of perforating eye injuries with intraocular foreign bodies. Acta Ophthalmol (Copenh) 1989;67:483–491. 5. Shock JP, Adams D. Long-term visual acuity results after penetrating and perforating ocular injuries. Am J Ophthalmol 1985;100:714–718. 6. Barak A, Elhalel A, Pikkel J, et al. Incidence and severity of ocular and adnexal injuries during the second Lebanon war among Israeli soldiers and civilians. Graefes Arch Clin Exp Ophthalmol 2011;249:1771–1774. 7. Yeh S, Colyer MH, Weichel ED. Current trends in the management of intraocular foreign bodies. Curr Opin Ophthalmol 2008;19:225–233. 8. Patel SN, Langer PD, Zarbin MA, Bhagat N. Diagnostic value of clinical examination and radiographic imaging in identification of intraocular foreign bodies in open globe injury. Eur J Ophthalmol 2012;22:259–268. 9. Gor DM, Kirsch CF, Leen J, et al. Radiologic differentiation of intraocular glass: evaluation of imaging techniques, glass types, size and effect of intraocular hemorrhage. AJR Am J Roentgenol 2001;177:1199–1203. 10. Kuhn F, Halda T, Witherspoon CD, et al. Intraocular foreign bodies: myths and truths. Eur J Ophthalmol 1996;6:464–471.
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