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The accuracy of wide-field ultrasound biomicroscopy in localizing extraocular rectus muscle insertions in strabismus reoperations
Accepted Manuscript The accuracy of wide-field ultrasound biomicroscopy in localizing extraocular rectus muscle insertions in strabismus reoperations Arash Mirmohammadsadeghi, MD, Vahideh Manuchehri, MD, Mohammad Reza Akbari, MD PII:
S1091-8531(17)30293-8
DOI:
10.1016/j.jaapos.2017.07.209
Reference:
YMPA 2696
To appear in:
Journal of AAPOS
Received Date: 14 April 2017 Revised Date:
15 July 2017
Accepted Date: 16 July 2017
Please cite this article as: Mirmohammadsadeghi A, Manuchehri V, Akbari MR, The accuracy of wide-field ultrasound biomicroscopy in localizing extraocular rectus muscle insertions in strabismus reoperations, Journal of AAPOS (2017), doi: 10.1016/j.jaapos.2017.07.209. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
The accuracy of wide-field ultrasound biomicroscopy in localizing extraocular rectus muscle insertions in strabismus reoperations Arash Mirmohammadsadeghi, MD, Vahideh Manuchehri, MD, and Mohammad Reza Akbari, MD
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Author affiliations: Eye Research Center, Farabi Eye Hospital, Tehran University of Medical Sciences, Tehran, Iran Submission received April 14, 2017. Revision accepted July 16, 2017.
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Correspondence: Mohammad Reza Akbari, MD, Farabi Eye Hospital, Ghazvin square, Tehran, Iran (email: [email protected]).
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Word count: 2,575 Abstract only: 253
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Abstract Purpose To compare the accuracy of widefield ultrasound biomicroscopy (UBM) with mechanical
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intraoperative measurements of the distance between rectus muscle insertions and the corneal limbus in strabismus reoperations. Methods
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Subjects with a history of horizontal rectus muscle surgery who required further surgery on
horizontal rectus muscle(s) were recruited prospectively. All widefield UBM measurements were
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carried out under topical anesthesia using a 50 MHz linear probe without immersion cup and external caliper. The insertion angle distance was measured using the caliper tool of the UBM device; the actual muscle insertion distance from the limbus was considered to be the measured distance plus 1 mm. The distance from muscle insertion to the limbus was also measured
Results
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intraoperatively. The results of UBM and surgical measurements were compared.
A total of 28 subjects were recruited, and 53 horizontal muscles (30 medial rectus, and 23 lateral
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rectus muscles) were included. The longest distance of the muscle insertion from limbus detectable on UBM was 13 mm for the medial rectus muscle and 15 mm for the lateral rectus
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muscle. In 38 muscles (71.7%) UBM and surgical measurements were within 1 mm of each other. Only in 1 muscle (1.9%) was the difference between measurements >2 mm (2.3 mm). The intraclass correlation coefficient was 0.87, demonstrating excellent agreement between measurements. Limit of agreement analysis demonstrated better agreement between measurments of medial rectus muscles and in consecutive exotropia cases. Conclusions
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This study demonstrated good agreement between intraoperative and widefield UBM
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measurements of the muscle insertion–limbus distance in our patient cohort.
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Localization of the extraocular muscle insertion is a challenging problem in eyes that have undergone previous strabismus surgeries. Information from the previous operation may be unavailable to the surgeon performing the reoperation. In addition, the limbus–insertion distance
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of rectus muscles can change over time because of enlargement of the eye or muscle slippage. Therefore, a method that preoperatively determines the distance between the rectus muscle insertion and limbus can improve planning for reoperations and decrease surgical time and
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possible complications.
Ultrasound biomicroscopy (UBM) is capable of imaging the anterior segment of the eye
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with high resolution.1 The accuracy of UBM in measuring the distance of insertion of extraocular muscles from the limbus in unoperated muscles has been demonstrated,2-5 but few studies address the accuracy of UBM in patients who previously underwent strabismus surgery.6,7 The purpose of this study was to determine the accuracy of widefield UBM in measuring the distance
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between rectus muscle insertions and the limbus in strabismus reoperations by comparing UBM and intraoperative measurements. Subjects and Methods
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This prospective, masked, observational study was performed in compliance with the Declaration of Helsinki and with the approval of the Farabi Eye Research Center Institutional
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Review Board. Written informed consent was obtained from all patients or guardians. Subjects with a history of horizontal rectus muscle surgery who required further surgery on one or more rectus muscles at the Farabi Eye Hospital from October 2015 to January 2017 were recruited. Patients with any anomalies in the limbus area, such as sclerocornea and corneal pannus, structural abnormalities, such as microphthalmia, or severely restricted eye movements were excluded, as were patients <12 years of age and any other subjects who could not tolerate UBM
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measurement under topical anesthesia. Age, sex, refractive error, amount of distance and near deviations, and type of deviation (consecutive exotropia, residual esotropia, and residual exotropia) were recorded for each case.
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Measurement Technique
Widefield UBM (Aviso, Quantel Medical, France) was used in this study. All UBM
measurements were made in the outpatient clinic by one examiner using the 50 MHz linear
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probe. The examiner was masked to details of the previous surgery. Under topical anesthesia and with the patient in the supine position, a lid speculum was inserted and tear gel was used as a
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coupling agent. The probe, without use of an immersion cup, was held on the scanned muscle, prependicular to the insertion. No external caliper was used during UBM measurement. The patient was asked to maintain gaze away from that muscle. After capture of a cross-section image, the termination of the cleft between muscle and sclera, appearing as a dark space on the
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image, was defined as the insertion.2 The anterior chamber angle was taken as a reference point. Using the caliper tool of the UBM device, the insertion angle distance was measured with a precision of 0.1 mm. Previous studies have stated that the anterior chamber angle was located
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approximately 1.0 mm posterior to the limbus.8 Therefore, the actual muscle insertion distance was considered as the measured distance plus 1 mm. Three images were taken and confirmed to
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be within 0.1 mm of each other; the mean of 3 measurement values was used in the analysis. The surgeon, who was masked to the UBM records, exposed the muscle insertion with
the muscle hook. Prior to each measurement, the accuracy of the caliper was confirmed against a ruler. The caliper was used to measure the distance from anterior part of the muscle hook to the limbus. Measurements were repeated, and the average of the two intraoperative measurements was recorded.
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Statistical Analysis Statistical analysis was performed using SPSS version 24 (SPSS corp, Armonk, NY). Categorical variables were recorded as numbers (percentages). Pearson correlation was used to
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evaluate the correlation between two sets. The intraclass correlation coefficient (ICC) was used to compare UBM and surgical measurements.9 Coefficient values of >0.8 were considered
excellent; values of 0.6-0.8 were considered good. In the last step, to assess agreement further,
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we used 95% limit of agreement (LOA) and Bland-Altman analysis. In the Bland-Altman
analysis, the difference between UBM and surgical measurements was plotted against the mean
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of 2 measurements.10 LOA shows the range between upper line (mean + 1.96 SDs of difference between 2 measurements) and lower line (mean − 1.96 SDs of difference between 2 measurements) in the Bland-Altman graph. The smaller the LOA range, the better the agreement between measurements is. In addition, if the maximum allowed difference between
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measurements is ±1 and the LOA range included ±1, the LOA results were not acceptable and the 2 methods did not have good agreement. On the other hand, if the clinically acceptable difference value was outside of the LOA range, the LOA results were acceptable and 2 methods
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had good agreements. The Loess method was used to determine whether there was any trend in the difference of the two sets with the change the average of the two sets.
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Results
A total of 53 horizontal muscles from 28 cases (15 male) were included. The mean age of subjects was 28.9 ± 9.8 (range, 13-50) years. The spherical part of refractive error was between −3.75 to +9.00. Seventeen cases (61%) were in the consecutive exotropia subgroup; 8 cases (29%), in the residual esotropia subgroup; and 3 cases (11%), in the residual exotropia subgroup. Mean preoperative deviation in primary position was 30.3∆ ± 14.2∆ (8-63) at distance and 32.0∆
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± 14.0∆ (10-63) at near fixation. A total of 30 medial rectus muscles and 23 lateral rectus muscles were evaluated by UBM. One of the captured UBM images is shown in Figure 1. The most posterior distance the
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muscle insertion was detected from limbus was 13 mm for the medial rectus muscle and 15 mm for the lateral rectus muscle.
In all previously recessed muscles, a pseudotendon was found intraoperatively as a
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fibrous tissue extending from original muscle insertion to the true insertion; on UBM imaging, the pseudotendon was detected clearly and differentiated from muscle in only 4 cases. In the
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UBM image, the potential space under the muscle was clearly visible as a black line. The space between pseudotendon and sclera was faint. Thus, in some cases the pseudotendon could be seen as a thin black line anterior to true muscle insertion in the UBM image. The statistics of UBM and surgery measurements in all cases and subgroups are provided
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in eTable 1. The mean distance of the insertion from limbus was 9.6 ± 1.6 mm (range, 6.2–13.9 mm) by UBM and 9.5 ± 1.9 mm (6.0–15.0) mm by surgical measurement. In 38 muscles (72%), both measurements were within 1 mm of each other. In 7 muscles (13%), the measurements were
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within 1–1.5 mm. In 7 muscles (13.2%), the measurements were within 1.5–2 mm. In 1 muscle (2%), the difference between measurements was 2.3 mm.
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The calculated ICC of 0.87 for all measurements indicates excellent agreement between
the two measurements. ICC was also calculated separately for medial rectus and lateral rectus muscles and deviation subgroups. The calculated ICCs for all subgroups were >0.8, again indicating excellent agreement. In addition, the Pearson coefficient (r) was 0.89 in all cases and >0.8 in the subgroups, showing very good agreement. As shown in the Bland-Altman graph in Figure 2, all measurements except 2 cases were
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within 1.96 standard deviations of the mean, indicating good agreement. The results of 95% LOA are provided in eTable 1. If the difference of ±1 mm is used as a clinically acceptable result, none of the LOA results will be acceptable; however, if the difference of ±2 mm is used as
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a clinically acceptable result, total, medial rectus muscle, and consecutive exotropia LOA results are acceptable. The residual esotropia subgroup also showed marginally acceptable LOA results (mean + 1.96 SD = 2.01), with the maximum allowed difference of ±2 mm.
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Discussion
In this study of a large cohort of patients requiring strabismus reoperations, a widefield 50 MHz
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UBM machine was used to detect the position of previously operated horizontal rectus muscles. To our knowledge, this is the first study on strabismus reoperations to assess widefield UBM imaging. Dai and colleagues6 performed their study using a Humphrey UBM. We used no caliper or immersion cup during UBM measurements, making the procedure easier for patients. We also
subgroups.
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report results of LOA analysis, which revealed particular effectiveness of the tool for some
The calculated ICC and Pearson coefficient demonstrated excellent agreement between
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UBM and surgical measurements. The longest distance of the muscle insertion from limbus detectable by UBM (13 mm for the medial rectus and 15 mm for the lateral rectus muscle) were
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more posterior than previously detected in all studies on UBM. Our study suggests that UBM is a useful tool for measuring the distance between limbus and rectus muscle insertions in reoperations.
Dai and colleagues6 used Humphrey UBM with external caliper in localizing 43 rectus
muscles under general and local anesthesia. In 80.5% of the cases, UBM and surgical measurements were within ± 1 mm of each other. The accuracy in measuring medial rectus and
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lateral rectus muscles did not differ. The limit of detection was 12 mm for the medial rectus muscle; 14 mm, for the lateral rectus muscle. Solarte and colleagues4 evaluated 24 unoperated and 7 operated vertical rectus muscles
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with Humphrey UBM and external caliper and reported very good agreement between the two methods (ICC = 0.78, Pearson coefficient = 0.85). The longest distance that UBM could measure was 12 mm. But they did not separate operated and unoperated muscles in the analysis.
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Khan and colleagues5 compared the new Sonomed widefield UBM with older Humphrey machine. The Sonomed did not need an external caliper if the muscle was within 14 mm of the
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limbus. They measured 40 unoperated and 10 operated horizontal and vertical muscles and used a silicone immersion cup for imaging. The ICC of 0.98 showed excellent correlation between the 2 readings. The results were better than that reported with the Humphrey UBM. As with the results of Solarte and colleagues,4 operated muscles were not separated from unoperated ones.
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The longest measured distance from the limbus was 12.19 mm.
Thakur and colleagues7 performed UBM imaging on 30 previously unoperated horizontal extraocular muscles preoperatively and repeated the UBM 3 months after surgery. They used the
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UBM OTI device (Ophthalmic Technologies, Toronto, Canada) with the immersion cup. Postoperatively, in 78.6% of MR muscles UBM and presumed postoperative position of the
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muscle were within 1 mm of each other. They found the lateral rectus muscle only in 50% of cases. In 62.5% of visible lateral rectus muscles, UBM and presumed postoperative position of the muscle were within 1 mm of each other. The longest distance measured by UBM was 11.2 mm for the medial rectus muscle and 13.5 mm for the lateral rectus. They concluded that UBM is not an accurate tool for postoperative muscle measurements. In our study the results of LOA analysis showed better accuracy of UBM for the medial
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rectus muscle. A similar finding was reported in Thakur and colleagues.7 An explanation for this result may be a shorter distance between the medial rectus muscle and the limbus, making detection of the medial rectus easier on UBM than detection of the lateral rectus muscle.
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Our analysis also indicated better accuracy of UBM for consecutive exotropia and
residual esotropia patients. This may be explained by the very low accuracy of UBM for recessed lateral rectus muscles compared to the high accuracy for recessed medial rectus and resected
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lateral rectus muscles. In Thakur and colleagues7 the accuracy of UBM for resected lateral rectus muscles and recessed medial rectus muscles was relatively good, but 8 of 11 recessed lateral
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rectus muscles were not detected by UBM.7 In the residual exotropia cases, the lateral rectus muscle had been previously recessed; therefore, the accuracy of UBM was decreased in this subgroup in their study.
Despite the high accuracy of UBM, there are some limitations in using it. UBM is an
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operator-dependent tool, and there may be inter- and intraexaminer variability in interpretation of results. Patient cooperation is necessary, and UBM cannot be performed in children and some cognitively impaired or anxious patients under topical anesthesia. Also, the muscle relaxant used
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in general anesthesia may change the size of the submuscular space and theoretically cause a posterior shift of the muscle insertion. Furthermore, UBM imaging cannot be performed in
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primary position and the distance of muscle from limbus may change with the patient’s gaze. There is no standard for quality of images, and conditions such as scar and fibrotic tissues, degree of eye movements, and size of palpebral fissure may affect image quality. Anterior segment optical coherence tomography (AS-OCT) is also used to measure
distance of insertion of extraocular muscles from the limbus.11-12 In contrast with UBM, ASOCT has the advantage of noncontact imaging, and imaging in awake children may be easier
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with AS-OCT. UBM and AS-OCT showed relatively similar accuracy in detecting unoperated muscles.11 But in reoperations, the accuracy of UBM may be better than AS-OCT.11 Rosetto and colleagues12 reported that the accuracy of AS-OCT was 58% in reoperations, in contrast with
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71.7% accuracy in our study. Therefore, UBM may be a better tool than AS-OCT to detect scarred muscles.
Our study was limited by the lack of comparison with other imaging modalities, such as
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anterior segment optical coherence tomography. In addition, no case of vertical muscle or
consecutive esotropia was found in our patients. Finally, in 28% of cases the difference between
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UBM and surgical measurements was >1 mm, a difference that may not be acceptable in some situations. Nevertheless, our results suggest that widefield UBM can be helpful in the preoperative assessments of patients with previous strabismus surgery and may thus facilitate surgical planning.
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Literature Search
PubMed, Scopus, and Embase after 1970 were searched on March 20, 2017, using the following topic-related keywords: ultrasound biomicroscopy AND strabismus, consecutive exotropia,
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residual exotropia, consecutive esotropia, and residual esotropia.
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References 1.
Pavlin CJ. Interpreting technology: practical application of ultrasound biomicroscopy.
2.
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Can J Ophthalmol 1995;30:225-9. Watts P, Smith D, Mackeen L, Kraft S, Buncic JR, Abdolell M. Evaluation of the ultrasound biomicroscope in strabismus surgery. J AAPOS 2002;6:187-90. 3.
Tamburrelli C, Salgarello T, Vaiano AS, Scullica L, Palombi M, Bagolini B. Ultrasound
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of the horizontal rectus muscle insertion sites: implications in preoperative assessment of
4.
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strabismus. Invest Ophthalmol Vis Sci 2003;44:618-22.
Solarte CE, Smith DR, Buncic JR, Tehrani NN, Kraft SP. Evaluation of vertical rectus muscles using Ultrasound Biomicroscopy. J AAPOS 2008;12:128-31.
5.
Khan HA, Smith DR, Kraft SP. Localizing rectus muscle insertions using high frequency wide-field ultrasound biomicroscopy. Br J Ophthalmol 2012;96:683-7. Dai S, Kraft SP, Smith DR, Buncic JR. Ultrasound biomicroscopy in strabismus
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6.
reoperations. J AAPOS 2006;10:202-5. 7.
Thakur N, Singh R, Kaur S, et al. Ultrasound biomicroscopy in strabismus surgery:
8.
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23:73-9.
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efficacy in postoperative assessment of horizontal muscle insertions. Strabismus 2015;
Park DJJ, Karesh JW. Chapter 1. Topographic anatomy of the eye: an overview. In: Tasman W, Jaeger EA, eds. Duane’s Foundations of Clinical Ophthalmology. Vol. 1. CD-ROM ed. Hagerstown, MD: Lippincott Williams & Wilkins, 2011.
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McGraw KO, Wong SP. Forming inferences about some intraclass correlation coefficients. Psychol Methods 1996;1:30-46.
10.
Bland JM, Altman DG. Statistical methods for assessing agreement between two methods
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of clinical measurement. Lancet 1986;1:307-10. 11.
Ngo CS, Smith D, Kraft SP. The accuracy of anterior segment optical coherence tomography (AS-OCT) in localizing extraocular rectus muscles insertions. J AAPOS
Rossetto JD, Cavuoto KM, Allemann N, McKeown CA, Capó H. Accuracy of optical coherence tomography measurements of rectus muscle insertions in adult patients
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undergoing strabismus surgery. Am J Ophthalmol 2017;176:236-43.
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12.
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2015;19: 233-6.
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Legends FIG 1. Ultrasound biomicroscopy (UBM) image of medial rectus muscle in a patient with consecutive exotropia. The line inserted by caliper tool of the machine shows the distance
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between angle and muscle insertion (9.9 mm in this case), and yields a distance of muscle
insertion from limbus of 10.9 mm. The true distance of the muscle insertion from the limbus, measured intraoperatively, was 11.5 mm.
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FIG 2. Bland-Altman graph showing the difference between UBM and surgical measurements plotted against average of UBM and surgical measurements. All measurements except 2 cases
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were within ± 2 standard deviations of the mean, indicating good agreement.
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eTable 1. The statistics of ultrasound biomicroscopy (UBM) measurement, surgical measurement, and the difference and absolute difference between the two variables in total cases and subgroups: Pearson coefficient (r), ICC, and 95% LOA are also provided Statistics
UBM
Muscle Medial Lateral Mean ± SD 9.6 ± 1.6 10.2 ± 1.5 8.9 ± 1.5 Median (IQR) 9.4 (8.4 to 10.8) 10.4 (9.4 to 11.2) 8.6 (8.1 to 9.1)
Residual ET 9.7 ± 1.4 9.4 (8.5 to 10.5)
Mean ± SD 9.5 ± 1.9 Median (IQR) 9.5 (8 to 11)
9.4 ± 1.7 9 (8 to 10.5)
10.2 ± 1.7 8.5 ± 1.8 10.7 (9.5 to 11.5) 8 (7.5 to 8.5)
Type of deviation Residual XT Consecutive XT 9.2 ± 3.7 9.6 ± 1.3 7.0 (6.4 to 12.7) 9.8 (8.6 to 10.8) 9.3 ± 4.3 6.5 (6 to 13)
9.5 ± 1.6 9.7 (8 to 11)
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surgery
Total
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Parameter
0.6 ± 0.4 0.8 ± 0.6 0.7 ± 0.5 0.5 (0.4 to 0.9) 0.6 (0.2 to 1.3) 0.6 (0.3 to 0.9) 23 (76.7%) 15 (65.2%) 11 (78.6%) 4 (13.3%) 3 (13.0%) 1 (7.1%) 3 (10.0%) 4 (17.4%) 2 (14.3%) 0 (0.0%) 1 (4.3%) 0 (0.0%) 0.89 0.84 0.86 0.88 0.83 0.85 −1.6 to 1.54 −1.55 to 2.33 −1.41 to 2.01
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a
UBM – surgery Mean ± SD 0.7 ± 0.5 Median (IQR) 0.5 (0.3 to 1.0) ≤1 38 (71.7%) 1-1.5 7 (13.2%) 1.5-2 7 (13.2%) 2+ 1 (1.9%) r 0.89 ICC 0.87 LOA −1.61 to 1.91
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UBM − surgery Mean ± SD 0.1 ± 0.9 −0.03 ± 0.8 0.3 ± 0.9 0.3 ± 0.8 −0.02 ± 1.3 0.12 ± 0.8 Median (IQR) 0.2 (−0.5 to 0.7) −0.1 (-0.5 to 0.5) 0.3 (-0.08 to 1.0) 0.4 (-0.03 to 0.7) 0.4 (-0.2 to 0.9) 0.06 (−0.5 to 0.5) 1 ± 0.7 0.7 ± 0.5 0.9 (0.4 to 1.0) 0.5 (0.2 to 1.0) 3 (60.0%) 24 (70.6%) 1 (20.0%) 5 (14.7%) 0 (0.0%) 5 (14.7%) 1 (20.0%) 0 (0.0%) 0.95 0.84 0.94 0.83 −2.69 to 2.65 −1.57 to 1.81
Absolute difference.
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a
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ET, esotropia; ICC, intraclass correlation coefficient; IQR, interquartile range; LOA, limits of agreement; SD, standard deviation; XT, exotropia.
S1091-8531(17)30293-8
DOI:
10.1016/j.jaapos.2017.07.209
Reference:
YMPA 2696
To appear in:
Journal of AAPOS
Received Date: 14 April 2017 Revised Date:
15 July 2017
Accepted Date: 16 July 2017
Please cite this article as: Mirmohammadsadeghi A, Manuchehri V, Akbari MR, The accuracy of wide-field ultrasound biomicroscopy in localizing extraocular rectus muscle insertions in strabismus reoperations, Journal of AAPOS (2017), doi: 10.1016/j.jaapos.2017.07.209. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT
The accuracy of wide-field ultrasound biomicroscopy in localizing extraocular rectus muscle insertions in strabismus reoperations Arash Mirmohammadsadeghi, MD, Vahideh Manuchehri, MD, and Mohammad Reza Akbari, MD
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Author affiliations: Eye Research Center, Farabi Eye Hospital, Tehran University of Medical Sciences, Tehran, Iran Submission received April 14, 2017. Revision accepted July 16, 2017.
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Correspondence: Mohammad Reza Akbari, MD, Farabi Eye Hospital, Ghazvin square, Tehran, Iran (email: [email protected]).
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Word count: 2,575 Abstract only: 253
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Abstract Purpose To compare the accuracy of widefield ultrasound biomicroscopy (UBM) with mechanical
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intraoperative measurements of the distance between rectus muscle insertions and the corneal limbus in strabismus reoperations. Methods
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Subjects with a history of horizontal rectus muscle surgery who required further surgery on
horizontal rectus muscle(s) were recruited prospectively. All widefield UBM measurements were
M AN U
carried out under topical anesthesia using a 50 MHz linear probe without immersion cup and external caliper. The insertion angle distance was measured using the caliper tool of the UBM device; the actual muscle insertion distance from the limbus was considered to be the measured distance plus 1 mm. The distance from muscle insertion to the limbus was also measured
Results
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intraoperatively. The results of UBM and surgical measurements were compared.
A total of 28 subjects were recruited, and 53 horizontal muscles (30 medial rectus, and 23 lateral
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rectus muscles) were included. The longest distance of the muscle insertion from limbus detectable on UBM was 13 mm for the medial rectus muscle and 15 mm for the lateral rectus
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muscle. In 38 muscles (71.7%) UBM and surgical measurements were within 1 mm of each other. Only in 1 muscle (1.9%) was the difference between measurements >2 mm (2.3 mm). The intraclass correlation coefficient was 0.87, demonstrating excellent agreement between measurements. Limit of agreement analysis demonstrated better agreement between measurments of medial rectus muscles and in consecutive exotropia cases. Conclusions
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This study demonstrated good agreement between intraoperative and widefield UBM
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SC
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measurements of the muscle insertion–limbus distance in our patient cohort.
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Localization of the extraocular muscle insertion is a challenging problem in eyes that have undergone previous strabismus surgeries. Information from the previous operation may be unavailable to the surgeon performing the reoperation. In addition, the limbus–insertion distance
RI PT
of rectus muscles can change over time because of enlargement of the eye or muscle slippage. Therefore, a method that preoperatively determines the distance between the rectus muscle insertion and limbus can improve planning for reoperations and decrease surgical time and
SC
possible complications.
Ultrasound biomicroscopy (UBM) is capable of imaging the anterior segment of the eye
M AN U
with high resolution.1 The accuracy of UBM in measuring the distance of insertion of extraocular muscles from the limbus in unoperated muscles has been demonstrated,2-5 but few studies address the accuracy of UBM in patients who previously underwent strabismus surgery.6,7 The purpose of this study was to determine the accuracy of widefield UBM in measuring the distance
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between rectus muscle insertions and the limbus in strabismus reoperations by comparing UBM and intraoperative measurements. Subjects and Methods
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This prospective, masked, observational study was performed in compliance with the Declaration of Helsinki and with the approval of the Farabi Eye Research Center Institutional
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Review Board. Written informed consent was obtained from all patients or guardians. Subjects with a history of horizontal rectus muscle surgery who required further surgery on one or more rectus muscles at the Farabi Eye Hospital from October 2015 to January 2017 were recruited. Patients with any anomalies in the limbus area, such as sclerocornea and corneal pannus, structural abnormalities, such as microphthalmia, or severely restricted eye movements were excluded, as were patients <12 years of age and any other subjects who could not tolerate UBM
ACCEPTED MANUSCRIPT
measurement under topical anesthesia. Age, sex, refractive error, amount of distance and near deviations, and type of deviation (consecutive exotropia, residual esotropia, and residual exotropia) were recorded for each case.
RI PT
Measurement Technique
Widefield UBM (Aviso, Quantel Medical, France) was used in this study. All UBM
measurements were made in the outpatient clinic by one examiner using the 50 MHz linear
SC
probe. The examiner was masked to details of the previous surgery. Under topical anesthesia and with the patient in the supine position, a lid speculum was inserted and tear gel was used as a
M AN U
coupling agent. The probe, without use of an immersion cup, was held on the scanned muscle, prependicular to the insertion. No external caliper was used during UBM measurement. The patient was asked to maintain gaze away from that muscle. After capture of a cross-section image, the termination of the cleft between muscle and sclera, appearing as a dark space on the
TE D
image, was defined as the insertion.2 The anterior chamber angle was taken as a reference point. Using the caliper tool of the UBM device, the insertion angle distance was measured with a precision of 0.1 mm. Previous studies have stated that the anterior chamber angle was located
EP
approximately 1.0 mm posterior to the limbus.8 Therefore, the actual muscle insertion distance was considered as the measured distance plus 1 mm. Three images were taken and confirmed to
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be within 0.1 mm of each other; the mean of 3 measurement values was used in the analysis. The surgeon, who was masked to the UBM records, exposed the muscle insertion with
the muscle hook. Prior to each measurement, the accuracy of the caliper was confirmed against a ruler. The caliper was used to measure the distance from anterior part of the muscle hook to the limbus. Measurements were repeated, and the average of the two intraoperative measurements was recorded.
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Statistical Analysis Statistical analysis was performed using SPSS version 24 (SPSS corp, Armonk, NY). Categorical variables were recorded as numbers (percentages). Pearson correlation was used to
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evaluate the correlation between two sets. The intraclass correlation coefficient (ICC) was used to compare UBM and surgical measurements.9 Coefficient values of >0.8 were considered
excellent; values of 0.6-0.8 were considered good. In the last step, to assess agreement further,
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we used 95% limit of agreement (LOA) and Bland-Altman analysis. In the Bland-Altman
analysis, the difference between UBM and surgical measurements was plotted against the mean
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of 2 measurements.10 LOA shows the range between upper line (mean + 1.96 SDs of difference between 2 measurements) and lower line (mean − 1.96 SDs of difference between 2 measurements) in the Bland-Altman graph. The smaller the LOA range, the better the agreement between measurements is. In addition, if the maximum allowed difference between
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measurements is ±1 and the LOA range included ±1, the LOA results were not acceptable and the 2 methods did not have good agreement. On the other hand, if the clinically acceptable difference value was outside of the LOA range, the LOA results were acceptable and 2 methods
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had good agreements. The Loess method was used to determine whether there was any trend in the difference of the two sets with the change the average of the two sets.
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Results
A total of 53 horizontal muscles from 28 cases (15 male) were included. The mean age of subjects was 28.9 ± 9.8 (range, 13-50) years. The spherical part of refractive error was between −3.75 to +9.00. Seventeen cases (61%) were in the consecutive exotropia subgroup; 8 cases (29%), in the residual esotropia subgroup; and 3 cases (11%), in the residual exotropia subgroup. Mean preoperative deviation in primary position was 30.3∆ ± 14.2∆ (8-63) at distance and 32.0∆
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± 14.0∆ (10-63) at near fixation. A total of 30 medial rectus muscles and 23 lateral rectus muscles were evaluated by UBM. One of the captured UBM images is shown in Figure 1. The most posterior distance the
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muscle insertion was detected from limbus was 13 mm for the medial rectus muscle and 15 mm for the lateral rectus muscle.
In all previously recessed muscles, a pseudotendon was found intraoperatively as a
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fibrous tissue extending from original muscle insertion to the true insertion; on UBM imaging, the pseudotendon was detected clearly and differentiated from muscle in only 4 cases. In the
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UBM image, the potential space under the muscle was clearly visible as a black line. The space between pseudotendon and sclera was faint. Thus, in some cases the pseudotendon could be seen as a thin black line anterior to true muscle insertion in the UBM image. The statistics of UBM and surgery measurements in all cases and subgroups are provided
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in eTable 1. The mean distance of the insertion from limbus was 9.6 ± 1.6 mm (range, 6.2–13.9 mm) by UBM and 9.5 ± 1.9 mm (6.0–15.0) mm by surgical measurement. In 38 muscles (72%), both measurements were within 1 mm of each other. In 7 muscles (13%), the measurements were
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within 1–1.5 mm. In 7 muscles (13.2%), the measurements were within 1.5–2 mm. In 1 muscle (2%), the difference between measurements was 2.3 mm.
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The calculated ICC of 0.87 for all measurements indicates excellent agreement between
the two measurements. ICC was also calculated separately for medial rectus and lateral rectus muscles and deviation subgroups. The calculated ICCs for all subgroups were >0.8, again indicating excellent agreement. In addition, the Pearson coefficient (r) was 0.89 in all cases and >0.8 in the subgroups, showing very good agreement. As shown in the Bland-Altman graph in Figure 2, all measurements except 2 cases were
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within 1.96 standard deviations of the mean, indicating good agreement. The results of 95% LOA are provided in eTable 1. If the difference of ±1 mm is used as a clinically acceptable result, none of the LOA results will be acceptable; however, if the difference of ±2 mm is used as
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a clinically acceptable result, total, medial rectus muscle, and consecutive exotropia LOA results are acceptable. The residual esotropia subgroup also showed marginally acceptable LOA results (mean + 1.96 SD = 2.01), with the maximum allowed difference of ±2 mm.
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Discussion
In this study of a large cohort of patients requiring strabismus reoperations, a widefield 50 MHz
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UBM machine was used to detect the position of previously operated horizontal rectus muscles. To our knowledge, this is the first study on strabismus reoperations to assess widefield UBM imaging. Dai and colleagues6 performed their study using a Humphrey UBM. We used no caliper or immersion cup during UBM measurements, making the procedure easier for patients. We also
subgroups.
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report results of LOA analysis, which revealed particular effectiveness of the tool for some
The calculated ICC and Pearson coefficient demonstrated excellent agreement between
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UBM and surgical measurements. The longest distance of the muscle insertion from limbus detectable by UBM (13 mm for the medial rectus and 15 mm for the lateral rectus muscle) were
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more posterior than previously detected in all studies on UBM. Our study suggests that UBM is a useful tool for measuring the distance between limbus and rectus muscle insertions in reoperations.
Dai and colleagues6 used Humphrey UBM with external caliper in localizing 43 rectus
muscles under general and local anesthesia. In 80.5% of the cases, UBM and surgical measurements were within ± 1 mm of each other. The accuracy in measuring medial rectus and
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lateral rectus muscles did not differ. The limit of detection was 12 mm for the medial rectus muscle; 14 mm, for the lateral rectus muscle. Solarte and colleagues4 evaluated 24 unoperated and 7 operated vertical rectus muscles
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with Humphrey UBM and external caliper and reported very good agreement between the two methods (ICC = 0.78, Pearson coefficient = 0.85). The longest distance that UBM could measure was 12 mm. But they did not separate operated and unoperated muscles in the analysis.
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Khan and colleagues5 compared the new Sonomed widefield UBM with older Humphrey machine. The Sonomed did not need an external caliper if the muscle was within 14 mm of the
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limbus. They measured 40 unoperated and 10 operated horizontal and vertical muscles and used a silicone immersion cup for imaging. The ICC of 0.98 showed excellent correlation between the 2 readings. The results were better than that reported with the Humphrey UBM. As with the results of Solarte and colleagues,4 operated muscles were not separated from unoperated ones.
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The longest measured distance from the limbus was 12.19 mm.
Thakur and colleagues7 performed UBM imaging on 30 previously unoperated horizontal extraocular muscles preoperatively and repeated the UBM 3 months after surgery. They used the
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UBM OTI device (Ophthalmic Technologies, Toronto, Canada) with the immersion cup. Postoperatively, in 78.6% of MR muscles UBM and presumed postoperative position of the
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muscle were within 1 mm of each other. They found the lateral rectus muscle only in 50% of cases. In 62.5% of visible lateral rectus muscles, UBM and presumed postoperative position of the muscle were within 1 mm of each other. The longest distance measured by UBM was 11.2 mm for the medial rectus muscle and 13.5 mm for the lateral rectus. They concluded that UBM is not an accurate tool for postoperative muscle measurements. In our study the results of LOA analysis showed better accuracy of UBM for the medial
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rectus muscle. A similar finding was reported in Thakur and colleagues.7 An explanation for this result may be a shorter distance between the medial rectus muscle and the limbus, making detection of the medial rectus easier on UBM than detection of the lateral rectus muscle.
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Our analysis also indicated better accuracy of UBM for consecutive exotropia and
residual esotropia patients. This may be explained by the very low accuracy of UBM for recessed lateral rectus muscles compared to the high accuracy for recessed medial rectus and resected
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lateral rectus muscles. In Thakur and colleagues7 the accuracy of UBM for resected lateral rectus muscles and recessed medial rectus muscles was relatively good, but 8 of 11 recessed lateral
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rectus muscles were not detected by UBM.7 In the residual exotropia cases, the lateral rectus muscle had been previously recessed; therefore, the accuracy of UBM was decreased in this subgroup in their study.
Despite the high accuracy of UBM, there are some limitations in using it. UBM is an
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operator-dependent tool, and there may be inter- and intraexaminer variability in interpretation of results. Patient cooperation is necessary, and UBM cannot be performed in children and some cognitively impaired or anxious patients under topical anesthesia. Also, the muscle relaxant used
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in general anesthesia may change the size of the submuscular space and theoretically cause a posterior shift of the muscle insertion. Furthermore, UBM imaging cannot be performed in
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primary position and the distance of muscle from limbus may change with the patient’s gaze. There is no standard for quality of images, and conditions such as scar and fibrotic tissues, degree of eye movements, and size of palpebral fissure may affect image quality. Anterior segment optical coherence tomography (AS-OCT) is also used to measure
distance of insertion of extraocular muscles from the limbus.11-12 In contrast with UBM, ASOCT has the advantage of noncontact imaging, and imaging in awake children may be easier
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with AS-OCT. UBM and AS-OCT showed relatively similar accuracy in detecting unoperated muscles.11 But in reoperations, the accuracy of UBM may be better than AS-OCT.11 Rosetto and colleagues12 reported that the accuracy of AS-OCT was 58% in reoperations, in contrast with
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71.7% accuracy in our study. Therefore, UBM may be a better tool than AS-OCT to detect scarred muscles.
Our study was limited by the lack of comparison with other imaging modalities, such as
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anterior segment optical coherence tomography. In addition, no case of vertical muscle or
consecutive esotropia was found in our patients. Finally, in 28% of cases the difference between
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UBM and surgical measurements was >1 mm, a difference that may not be acceptable in some situations. Nevertheless, our results suggest that widefield UBM can be helpful in the preoperative assessments of patients with previous strabismus surgery and may thus facilitate surgical planning.
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Literature Search
PubMed, Scopus, and Embase after 1970 were searched on March 20, 2017, using the following topic-related keywords: ultrasound biomicroscopy AND strabismus, consecutive exotropia,
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residual exotropia, consecutive esotropia, and residual esotropia.
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References 1.
Pavlin CJ. Interpreting technology: practical application of ultrasound biomicroscopy.
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Can J Ophthalmol 1995;30:225-9. Watts P, Smith D, Mackeen L, Kraft S, Buncic JR, Abdolell M. Evaluation of the ultrasound biomicroscope in strabismus surgery. J AAPOS 2002;6:187-90. 3.
Tamburrelli C, Salgarello T, Vaiano AS, Scullica L, Palombi M, Bagolini B. Ultrasound
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of the horizontal rectus muscle insertion sites: implications in preoperative assessment of
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strabismus. Invest Ophthalmol Vis Sci 2003;44:618-22.
Solarte CE, Smith DR, Buncic JR, Tehrani NN, Kraft SP. Evaluation of vertical rectus muscles using Ultrasound Biomicroscopy. J AAPOS 2008;12:128-31.
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Khan HA, Smith DR, Kraft SP. Localizing rectus muscle insertions using high frequency wide-field ultrasound biomicroscopy. Br J Ophthalmol 2012;96:683-7. Dai S, Kraft SP, Smith DR, Buncic JR. Ultrasound biomicroscopy in strabismus
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reoperations. J AAPOS 2006;10:202-5. 7.
Thakur N, Singh R, Kaur S, et al. Ultrasound biomicroscopy in strabismus surgery:
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23:73-9.
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efficacy in postoperative assessment of horizontal muscle insertions. Strabismus 2015;
Park DJJ, Karesh JW. Chapter 1. Topographic anatomy of the eye: an overview. In: Tasman W, Jaeger EA, eds. Duane’s Foundations of Clinical Ophthalmology. Vol. 1. CD-ROM ed. Hagerstown, MD: Lippincott Williams & Wilkins, 2011.
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McGraw KO, Wong SP. Forming inferences about some intraclass correlation coefficients. Psychol Methods 1996;1:30-46.
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Bland JM, Altman DG. Statistical methods for assessing agreement between two methods
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of clinical measurement. Lancet 1986;1:307-10. 11.
Ngo CS, Smith D, Kraft SP. The accuracy of anterior segment optical coherence tomography (AS-OCT) in localizing extraocular rectus muscles insertions. J AAPOS
Rossetto JD, Cavuoto KM, Allemann N, McKeown CA, Capó H. Accuracy of optical coherence tomography measurements of rectus muscle insertions in adult patients
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undergoing strabismus surgery. Am J Ophthalmol 2017;176:236-43.
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12.
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2015;19: 233-6.
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Legends FIG 1. Ultrasound biomicroscopy (UBM) image of medial rectus muscle in a patient with consecutive exotropia. The line inserted by caliper tool of the machine shows the distance
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between angle and muscle insertion (9.9 mm in this case), and yields a distance of muscle
insertion from limbus of 10.9 mm. The true distance of the muscle insertion from the limbus, measured intraoperatively, was 11.5 mm.
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FIG 2. Bland-Altman graph showing the difference between UBM and surgical measurements plotted against average of UBM and surgical measurements. All measurements except 2 cases
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were within ± 2 standard deviations of the mean, indicating good agreement.
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eTable 1. The statistics of ultrasound biomicroscopy (UBM) measurement, surgical measurement, and the difference and absolute difference between the two variables in total cases and subgroups: Pearson coefficient (r), ICC, and 95% LOA are also provided Statistics
UBM
Muscle Medial Lateral Mean ± SD 9.6 ± 1.6 10.2 ± 1.5 8.9 ± 1.5 Median (IQR) 9.4 (8.4 to 10.8) 10.4 (9.4 to 11.2) 8.6 (8.1 to 9.1)
Residual ET 9.7 ± 1.4 9.4 (8.5 to 10.5)
Mean ± SD 9.5 ± 1.9 Median (IQR) 9.5 (8 to 11)
9.4 ± 1.7 9 (8 to 10.5)
10.2 ± 1.7 8.5 ± 1.8 10.7 (9.5 to 11.5) 8 (7.5 to 8.5)
Type of deviation Residual XT Consecutive XT 9.2 ± 3.7 9.6 ± 1.3 7.0 (6.4 to 12.7) 9.8 (8.6 to 10.8) 9.3 ± 4.3 6.5 (6 to 13)
9.5 ± 1.6 9.7 (8 to 11)
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surgery
Total
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Parameter
0.6 ± 0.4 0.8 ± 0.6 0.7 ± 0.5 0.5 (0.4 to 0.9) 0.6 (0.2 to 1.3) 0.6 (0.3 to 0.9) 23 (76.7%) 15 (65.2%) 11 (78.6%) 4 (13.3%) 3 (13.0%) 1 (7.1%) 3 (10.0%) 4 (17.4%) 2 (14.3%) 0 (0.0%) 1 (4.3%) 0 (0.0%) 0.89 0.84 0.86 0.88 0.83 0.85 −1.6 to 1.54 −1.55 to 2.33 −1.41 to 2.01
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UBM – surgery Mean ± SD 0.7 ± 0.5 Median (IQR) 0.5 (0.3 to 1.0) ≤1 38 (71.7%) 1-1.5 7 (13.2%) 1.5-2 7 (13.2%) 2+ 1 (1.9%) r 0.89 ICC 0.87 LOA −1.61 to 1.91
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UBM − surgery Mean ± SD 0.1 ± 0.9 −0.03 ± 0.8 0.3 ± 0.9 0.3 ± 0.8 −0.02 ± 1.3 0.12 ± 0.8 Median (IQR) 0.2 (−0.5 to 0.7) −0.1 (-0.5 to 0.5) 0.3 (-0.08 to 1.0) 0.4 (-0.03 to 0.7) 0.4 (-0.2 to 0.9) 0.06 (−0.5 to 0.5) 1 ± 0.7 0.7 ± 0.5 0.9 (0.4 to 1.0) 0.5 (0.2 to 1.0) 3 (60.0%) 24 (70.6%) 1 (20.0%) 5 (14.7%) 0 (0.0%) 5 (14.7%) 1 (20.0%) 0 (0.0%) 0.95 0.84 0.94 0.83 −2.69 to 2.65 −1.57 to 1.81
Absolute difference.
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ET, esotropia; ICC, intraclass correlation coefficient; IQR, interquartile range; LOA, limits of agreement; SD, standard deviation; XT, exotropia.