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Keywords:

  • contrast;
  • enhancement;
  • extra-ocular;
  • muscle;
  • MRI

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

Enhancement of extra-ocular muscles has been reported in cases of orbital pathology in both veterinary and medical magnetic resonance imaging. We have also observed this finding in the absence of orbital disease. The purpose of this retrospective study was to describe extra-ocular muscle contrast enhancement characteristics in a group of dogs with no known orbital disease. Magnetic resonance images (MRI) from dogs with no clinical evidence of orbital disease and a reportedly normal MRI study were retrieved and reviewed. Contrast enhancement percentages of the medial, lateral, ventral, and dorsal rectus muscles were calculated based on signal-to-noise ratios that were in turn determined from hand-traced regions of interest in precontrast, immediate postcontrast and 10-min postcontrast scans. Comparison measurements were made in the pterygoid muscle. Contrast enhancement of the extra-ocular muscles was observed in all patients (median contrast enhancement percentage 45.0%) and was greater than that of pterygoid muscle (median contrast enhancement percentage 22.7%). Enhancement of the extra-ocular muscles persisted 10 min after contrast administration (median contrast enhancement percentage 43.4%). Findings indicated that MRI contrast enhancement of extra-ocular muscles is likely normal in dogs.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

Magnetic resonance imaging (MRI) of the orbit and peri-orbital structures is used routinely in the diagnostic work up of many ophthalmological conditions.[1-5] The superior soft tissue contrast resolution and multiplanar acquisition allow detailed lesion detection and understanding of the complex anatomical structures of the orbit.[4, 6] Contrast administration, using gadolinium chelates, improves the detection of pathological processes in MRI.[7] However, highly vascular normal structures may also show marked enhancement following contrast administration and may mask, or even appear as, pathological processes.[8-10] Contrast enhancement of extra-ocular muscles has been reported in canine cases of suspected inflammatory diseases such as extra-ocular polymyositis, masticatory myositis, or peri-orbital cellulitis.[1, 3, 5] However, at our practice, contrast enhancement of extra-ocular muscles has also been seen in canine cases without orbital disease. Contrast enhancement of extra-ocular muscles has been reported to be a normal finding in human MRI but, to the author's knowledge, this has not been documented in the veterinary literature.[11, 12] The purpose of this retrospective study was to describe the contrast enhancement characteristics of extra-ocular muscles in a group of dogs with no known orbital disease.

Materials and Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

Dogs with no clinical signs or history of orbital disease and that had MRI examinations of the head between December 2009 and May 2010 were included in the study. Dogs were excluded if there were any abnormalities in hematology, serum biochemistry or cerebrospinal fluid analysis, and if the MRI examination revealed any abnormalities or if post contrast MRI sequences were unattainable.

All MRI data were acquired using a 1.5 Tesla scanner (Siemens Magnetom Essenza, Siemens AG, Erlangen, German) with a human head/neck coil. For all dogs, T2-weighted sagittal, dorsal, and transverse; FLAIR transverse; T2*-gradient echo transverse and T1-weighted transverse sequences were acquired. The T1-weighted transverse sequences (TR = 455–674 ms, TE = 13) were repeated immediately following contrast medium administration and again 10 min later to assess persistence of contrast enhancement over time. Transverse plane slice thicknesses were either 3 or 4 mm depending on patient size.

Baseline, immediate post contrast (1 min) and delayed post contrast (10 min) T1-weighted images were analyzed using a DICOM image viewer (OsiriX version 5.5, OsiriX Imaging Software, OsiriX Foundation, Geneva, Switzerland). Regions of interest were manually traced around the medial rectus, lateral rectus, ventral rectus, dorsal rectus, and pterygoid muscles of the left and right eyes for the baseline and two postcontrast series. All regions of interest were placed at a slice location where the muscles appeared most perpendicular to the slice plane (Fig 1). An additional external air space region of interest was collected from each T1-weighted sequence and used to calculate signal noise. Each rectus muscle was identified based on their respective location within the orbit and the presence of surrounding infra-orbital fat.[6, 13] The pterygoid muscle was identified lateral to the pterygoid process, and regions of interest for this muscle were traced in the same image slice as the extra-ocular muscle regions of interest. Regions of interest were linked between T1-weighted sequences using point-based registration. The mean signal intensity (SI) and standard deviation (SD) were recorded for each region of interest, in arbitrary units.

image

Figure 1. Transverse T1-weighted gadolinium contrast-enhanced image of the head at the level of the orbit. (A); Medial rectus muscle, (B); Lateral rectus muscle, (C); Ventral rectus muscle, (D); Dorsal rectus muscle, (E); Pterygoid muscle (left lateral aspect labeled).

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For each region of interest, the mean signal-to-noise ratio (SNR) was calculated using the following formula: SNR = (SItissue/SDair). Enhancement percentage (E%) of each region of interest for both postcontrast sequences was calculated using the following formula: E% = (SNRpost–SNRbaseline)/SNRbaseline

Statistical analyses were performed using commercial software (SPSS 19.0 (SPSS Inc., Chicago, IL USA). The distribution of the data was evaluated using the Shapiro–Wilk test, skewness, kurtosis, and q-q plots. Non-normally distributed data were log transformed for parametric analysis. Data that were normally distributed were reported by the mean, SD, and minimum–maximum values (min–max), while non-normally distributed data were reported by the median, 10–90%, and minimum–maximum. A repeated measures analysis of variance (ANOVA) was used to compare SNRs and E% over time (within subject) while controlling for eye (between subject). Mauchly's test was used to determine sphericity. If sphericity was violated, the Greenhouse–Geisser test was used. When there was a significant difference detected over time, the Bonferonni post-hoc test was used to identify the difference. Statistical significance for all tests was defined as P < 0.05.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

A total of 22 dogs were included in the current study. These dogs had been also included in a previously published study on delayed MRI contrast enhancement characteristics of the brain in dogs with no clinical evidence of intracranial disease.[8] Ages ranged from 8 months to 10 years, with a mean of 4.4 years. Five of 12 males were intact and three of 10 females were entire. The majority were mixed-breed dogs (N = 4), Labrador retrievers (N = 3), Dalmatians (N = 2), Jack Russell terriers (N = 2), Shih-Tzus (N = 2), and Boxers (N = 2).

There was no significant difference in SNRs between the left and right eyes for all muscles in each T1-weighted series (medial rectus F = 1.1, P = 0.29; lateral rectus F = 0.9, P = 0.91; ventral rectus F = 0.3, P = 0.57; dorsal rectus F = 0.4, P = 0.52; and pterygoid F = 0.01, P = 0.99). The SNRs of muscles (combined laterality) in each T1-weighted series are displayed in Fig. 2.

image

Figure 2. Signal-to-noise ratio for each muscle (combined laterality): baseline series, 1 min post contrast, 10 min post contrast. * – Denotes no significant difference for the specified region of interest between the two postcontrast series. Pt, pterygoid; MR, medial rectus; LR, lateral rectus; VR, ventral rectus; DR, dorsal rectus.

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Overall, there was a significant difference in SNRs in each muscle group over time (F = 392.4, P = 0.0001), as well as a significant difference between extraocular (combined) vs. pterygoid muscles (F = 138.7, P = 0.0001; Table 1).

Table 1. Extra-Ocular and Pterygoid Signal-to-Noise Ratios Calculated Over Time, by Muscle Type
Signal-to-noise ratio over time   
by muscle type (combined   
ocular vs. pterygoid)Median10–90%Minimum–Maximum
Baseline   
Extra-ocular21.716.9–26.114.2–31.8
Pterygoid18.113.6–19.911.9–21.8
1 minute post contrast   
Extra-ocular31.224.1–38.919.2–55.1
Pterygoid22.216.6–24.514.6–32.5
10 minute post contrast   
Extra-ocular30.424.6–37.821.7–50.0
Pterygoid2116.3–23.814.5–29.4

The enhancement percentage of the muscles (combined laterality) in each postcontrast T1-weighted series is displayed in Fig. 3. There were significant differences in contrast enhancement between extraocular (combined) vs. pterygoid muscles at both postcontrast times (1 min P = 0.0001 and 10 min P = 0.0001; Table 2).

Table 2. Contrast Enhancement% by Muscle Type (Combined vs. Pterygoid)
CE% over time by muscle type   
(combined ocular vs. pterygoid).Median10–90%Minimum–Maximum
1 minute post contrast   
Ocular45.023.9–71.82.0–117.0
Pterygoid22.715.4–32.74.0–53.0
10 minute post contrast   
Ocular43.429.7–58.47.0–91.0
Pterygoid18.19.1–26.00 – 38.0
image

Figure 3. Contrast enhancement percentage at 1 min (white) and 10 min (striped) postcontrast administration. * – Denotes no significant difference for the specified region of interest between the two postcontrast series. Pt, pterygoid; MR, medial rectus; LR, lateral rectus; VR, ventral rectus; DR, dorsal rectus.

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES

Despite previous studies reporting MRI contrast enhancement of the extra-ocular muscles representing pathology, such as myositis or neoplasia, quantitative assessment of the contrast enhancement of these muscles has not previously been reported.[1, 4, 5] This MRI study identified significant contrast enhancement of extra-ocular muscles following contrast administration in the absence of clinical evidence of ocular pathology.

All extra-ocular muscles had a significantly higher overall SNR and enhancement percentage following contrast administration compared to the pterygoid muscle. Authors acknowledge that pathologic confirmation of normal muscle status was not performed, therefore the possibility of subclinical disease cannot be completely excluded. However, this finding was consistent with previous human imaging reports that found enhancement of the extra-ocular muscles to be a normal feature.[11, 12] One human study looked at the histological basis for increased contrast enhancement in extra-ocular muscles and found that the rich vascularity and prominent extra-vascular spaces are likely responsible for the marked enhancement following gadolinium contrast administration.[12] The difference in contrast enhancement of extra-ocular muscles vs. that of non-ocular skeletal muscle has been proposed to be due to the highly specialized function of the extra-ocular muscles allowing rapid conjugate, high-speed precision movements and sustained, nonfatiguing tonus.[12] The pterygoid was selected to represent nonocular skeletal muscle in the current study for comparison due to the close proximity to the orbit on transverse MRI images. The SNRs and enhancement characteristics of the pterygoid muscle in the current study were consistent with other previous studies describing nonocular skeletal muscle enhancement over time.[8, 14]

The immediate and delayed postcontrast series in our study showed no significant differences in SNR or enhancement percentage for either the medial rectus or lateral rectus muscles. The large extravascular spaces of these extra-ocular muscles were thought to contribute to the prolonged enhancement over time.[12] Significant differences over time were, however, seen for the ventral rectus and dorsal rectus muscles. The authors speculate that the lack of retained enhancement seen in these muscles relates to a variable, but minor, dorso-ventral rotation/relaxation of the extra-ocular muscles during the time of scanning.

Fat suppression techniques used in a previous subjective study of human ocular MRI[11] were not deemed necessary in our study as the assessment was performed objectively using regions of interest matched across sequences by a point based registration. Our study was also performed retrospectively and primarily included patients undergoing assessment for intracranial disease. Fat-suppressed techniques are not routinely used for these examinations. Adipose tissue may increase the baseline SNR if inadvertently included in the region of interest, but the enhancement percentage should not be affected as it represents differences in the T1-weighted sequences.

In conclusion, findings from the current study indicated that contrast enhancement of the canine extra-ocular muscles may be a normal finding, and the presence should not be used alone as a feature of orbital pathology. Signal-to-noise ratios and contrast enhancement percentages for each extra-ocular muscle are provided for use as references in future imaging studies assessing orbital pathology.

REFERENCES

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and Methods
  5. Results
  6. Discussion
  7. REFERENCES