This study demonstrates the potential of high-field MRI in an ophthalmology setting for visualizing normal anterior segment anatomy. Unlike other well-established ophthalmological imaging methods, MRI provides true anatomic proportions independent of the optical and absorption characteristics of the ocular tissues. Earlier published in vivo studies
13 –15,19 –24 using 1.5 T MR imagers have shown an SNR resulting in limited resolution. Surface coils of various configurations have been used in the past, for example, to investigate anatomy,
19 intraocular metastases,
20 ocular and orbital lesions,
21 as well as extraocular muscles.
22 MRI has been used to observe the relationship between ciliary muscle activity and lens response,
10,13,23,24 changes in lens volume during accommodation,
14 and cataractous lens changes.
25 Richdale et al.
17 have developed protocols that optimize contrast, resolution, and scan time for three-dimensional imaging of the human eye in vivo using a 7 T scanner. The Miyake-Apple technique, video analysis, and MRI have been used to investigate anterior segment structures after surgical manipulation of postmortem eyes.
15 Recent accommodation studies using MRI are quite rare compared with those using optical and ultrasound technologies.
One drawback with the studies cited above is the limited SNR with 1.5 T MR systems. Although 1.5 T MR scanners provide good contrast, spatial resolution, and detail, they offer inferior SNR when compared with ultra-high-field MRI. The MRI method developed by Strenk et al.
10,23,24,26 for in vivo imaging of the anterior segment provides an FoV of 40 × 40 mm and in-plane resolution of 156 × 156 μm
26 and 78 × 78 μm,
23 respectively. Using 7.1 T and T2w TSE sequences, it was possible to achieve in-plane resolution of 80 × 80 μm ex vivo and 125 × 125 μm in vivo when imaging the anterior and posterior segments of the eye.
Consequently, although the theoretical in-plane resolution for this study using 7.1 T is almost comparable with that in the 1.5 T studies conducted by Strenk, there is greater SNR. Therefore, the image information with 7.1 T appears far more detailed. The anterior segment cross-sections presented in
Figures 5 and
6 confirm this conclusion. In addition, there was no alteration of image quality because of eye movements, microsaccades, for example, when ex vivo imaging was performed. Similarly, artifacts due to eye movements were also not an issue when in vivo imaging was performed under general anesthesia. Ex vivo imaging not only allows the coil to be placed closer to the surface of the cornea, but also reduces artifacts caused by the lid, a complication encountered in previous in vivo studies of the human eye
17 .
Compared with laser techniques and Scheimpflug imaging, micro-MRI is not superior and offers no improvement for determining axial LT or imaging the central radius of curvature. However, the advantage of high-field MRI technology, which has the capability of 3D image and data analysis, is that it reveals overall lens geometry in relation to ciliary body configuration and lens volume. A full set of biometric data is shown in
Table 2 for the different species to illustrate the potential of ultra-high-field MRI. This is applicable for both crystalline lenses as well as intraocular lenses (although data on the latter are not presented here). This demonstrates the advantage of MRI over optical and ultrasound methods. Again, the capability to acquire the entire lens shape rather than part of it may yield more precise knowledge about lens volume and the principal lens dimensions, including radius of curvature. For instance, overall lens dimensions in relation to sulcus-sulcus distance are important in regard to new IOL implants designed to correct presbyopia.
Ultrasound and MRI-based LT determinations were compared to identify the correlation between these two methods. A systematic difference (mean, 120 μm) was detected, with higher values for US (
Fig. 7;
Table 4). This 3% offset may be due to a variety of factors, such as sound velocity for US, ultrasound transducer alignment, or tilt of MRI cross-sections. However, the systematic offset is more suggestive of a systematic error, and any future study must include a larger set of samples to permit detailed analysis of this phenomenon. The SD on ultrasound-based LT determination is comparable to that based on MRI data (SD
US = 0.030 mm, SD
MRI = 0.035 mm). No significant differences were detected between 7.1 T MRI and A-scan US in terms of LT determinations in monkey eyes (
P > 0.05, Mann–Whitney
U test). It can therefore be concluded that a micro-MRI–based quantitative analysis of anterior segment dimensions is comparable to that based on A-scan US.
Use of color-coded gradient field maps enabled the visualization of the homogeneity of the local magnetic field within the eye. Together with the linearity of the magnetic gradients used for imaging, this is the major prerequisite for obtaining true anatomic proportions without optical distortion. This has been demonstrated clearly in practice by comparing the IOL manufacturer's optic data with the MR image of a pseudophakic monkey eye (
Fig. 8). In-plane distances are identical, and a circular arc with the exact radius of curvature is closely aligned with the posterior spherical surface of the IOL. This analysis confirms the absence of relevant distortion artifacts inside the MR images. Coincidentally, micro-MRI offers astonishingly high repeatability, as demonstrated by LT determinations. Repeated scanning on the same eye resulted in a SD of approximately 0.14 mm, equivalent to <2 pixels in plane.
One limitation of ultra-high-field MRI with surface coils
18 is the signal drop-off from the surface of the coil to the center of the vitreous body. The same limitation was described by Richdale et al.
17 and is also known from previous studies at 1.5 T. For imaging the anterior segments of the eye, surface coils are preferable and provide excellent SNR.
Increasing the strength of the static magnetic field and the gradients could theoretically lead to radio frequency (RF)-induced heating of tissue, with the attendant potential for altering contrast. RF-induced temperature changes might alter T1 and T2 values of the tissue investigated. Temperature was therefore monitored ex vivo in a pig eye during a T2w TSE sequence, revealing a slight temperature increase, as assessed with a fiber optic probe placed in the anterior chamber. The probe is immune to electromagnetic- and radio frequency–induced interferences, and temperature measured with this probe is caused only by the RF-induced tissue heating of the probe itself. A temperature increase in the anterior chamber of 0.6°C was found during a 9.18 minute T2w high-resolution scan sequence. These temperature changes observed in this study did not lead either to cross-contrast changes or to geometrical distortions, and this was demonstrated by the results of the reproducibility studies. These findings are supported by the work of Richdale et al.,
17 who did not observe changes in T1 values during imaging of the human eye in vivo at 7 T.
The published in vivo studies cited above, in combination with the ex vivo and in vivo animal and donor eye studies presented here, demonstrate the future potential of high-field MRI for enhancing biomechanical understanding and the biometric evaluation of the crystalline lens and of artificial intraocular lenses. At present, particularly for humans, access to this technology is still limited because of the small tube diameter; however, new high-field systems are opening fresh horizons in intraocular imaging. In the future, ultra-high-resolution MRI will become an extremely useful modality that permits visualization of the relationship between ciliary muscle activity and lens response, including the circumlental space. The present study lends weight to the body of opinion that micro-MRI technology should be introduced into anterior segment imaging and justifies the investment of further efforts to establish this technology in experimental and clinical ophthalmology. This novel approach to exploring the anterior segment of the eye yields high-resolution images without optical distortion and overcomes many of the major limitations that are a feature of other quantitative imaging modalities.
Supported in part by the DFG (Transregio 37, Micro- and Nanosystems in Medicine—Reconstruction of Biological Functions), KüAkk
REMEDIS, and SenterNovem Dutch Grant IS043081.
The authors acknowledge the contribution of Tim Wokrina (Bruker BioSpin, Germany) for providing the fiber optic thermometer and Helga Krentz for statistical advice.