Introduction

Ultrasound biomicroscopy (UBM) systems are suitable for imaging of virtually all aspects of anterior segment including the cornea, anterior chamber, iris and iridocorneal angle, ciliary body and lens (Chapter 4). Ultrasound is therefore applicable to a host of corneal disorders. Although anterior segment examinations are most commonly performed with a fluid-filled scleral shell, they may also utilize a water bath or a membrane-enclosed tip applied to the eye after topical anesthetic. A gentle through-the-lid approach is most commonly used in cases of trauma, albeit at the cost of reduced sensitivity due to attenuation by the lids (Chapter 3).^1,2

Pavlin et al were the first to describe UBM imaging of the cornea.^2,3 Diagnostic uses in the setting of corneal pathology include congenital corneal opacification, edema,⁴ keratoconus,^5,6 dystrophies,⁷ corneal scars,^8,9 trauma,¹⁰ and corneal keloid.¹¹

The earliest commercial UBM system from Zeiss-Humphrey (later Paradigm Medical Industries, Salt Lake City, UT, USA) consisted of a handheld 50 MHz probe that allowed unparalleled non-invasive imaging of anatomic areas of interest throughout the anterior segment. Later generation handheld systems from several manufacturers offer higher scan rates and more compact probes.¹ An automated high frequency ultrasound system developed at Cornell University and commercialized as the Artemis-2 (ArcScan) couples a disposable water bath interface and an arcuate probe scanning pathway that approximates normality between the ultrasound beam axis and the corneal surface to facilitate corneal biometric analysis with sufficient scan width to visualize the anterior segment from sulcus to sulcus (Chapter 6). The Artemis very high frequency digital ultrasound system (bandwidth 10 to 60 MHz) has advantages over analog processing systems in its ability to consistently detect internal corneal interfaces due to the higher signal-to-noise ratio between the interface echo complex and the surrounding tissue. These sensitivity gains and a more systematic measurement approach favor excellent quantitative repeatability for small ocular structures such as corneal sublayers compared to UBM.¹² Optical coherence tomography (OCT), an interferometric technique first described by Huang et al in 1991,¹³ has also been shown to be capable of detecting corneal sublayer interfaces such as the laser in-situ keratomileusis (LASIK) flap in the early postoperative period.¹⁴ A limitation of OCT is its inability to image the ciliary sulcus through the iris.

Cornea

Normal cornea

Previous studies have shown that the corneal imaging is best conducted with 80–100-MHz probes because the axial resolution is directly proportional to the emission frequency. Pavlin et al showed that even with high-frequency probes, the cornea appears to be divided into four layers rather than its true five layers.^2,3

The first layer encountered by an acoustic signal is the epithelium, which is approximately 50 µm thick and has a slightly irregular anterior surface. Bowman’s layer is visible under the epithelium as a highly reflective continuous line because of several interfaces within it. It should be noted that these two layers are not always clearly distinguishable with a 50-MHz probe and can be better identified by post-processing of the signal.^2–4

With a more regular internal lamellar structure, the corneal stroma appears as a uniform layer with medium to low reflectivity. This is in contrast to the sclera and Bowman’s layer, which are more reflective because of the more irregular arrangement of collagen fibrils. The fourth layer is represented by Descemet’s membrane (DM) and the endothelial monolayer, which cannot be visualized as two distinct layers and therefore appear as a highly reflective continuous line behind the stroma (Figure 8.1).^2–4

Figure 8.1 Normal cornea imaged with 50 MHz analogue UBM system (A). Non-geometrically corrected horizontal Artemis B-scan (B, above) and horizontal Visante OCT B-scan (B, below) of the same eye. Superimposed on the Artemis B-scan is the I-scan derived by digital processing of the radio frequency ultrasonic B-scan data from which the measurements are obtained. The I-scan demonstrates sharp distinct peaks representing the acoustic interfaces of saline-epithelium (E), epithelium-Bowman’s (B), the lamellar interface (I), and the endothelial-aqueous interface (P).

Figure B is courtesy of Dan Z. Reinstein, MD, London, UK.

Congenital corneal opacity

UBM is useful not only for determining the clinical diagnosis in congenital corneal opacification, but also for refining the surgical plan before keratoplasty where keratolenticular and iridocorneal adhesions and other ocular abnormalities such as aniridia and congenital aphakia are detected.¹⁵

Nischal et al studied the correlation of ultrasound biomicroscopy and histological findings in cases of congenital corneal opacification.¹⁵ In a report of 22 eyes in 13 patients who were diagnosed with Peter’s anomaly, corneal dystrophy, and sclerocornea, UBM findings changed the final diagnosis in 5 of the 13 cases. They showed that the usually contiguous reflectivity of the DM/endothelium layer seen on UBM was instead irregular, a finding confirmed on histology to be due to focal absences of Descemet’s membrane with multilayering of the endothelium in cases of posterior polymorphous dystrophy (PPMD) and absence of endothelium in cases of congenital hereditary endothelial dystrophy (CHED). Similarly, the presence of a hypoechoic layer in the anterior stroma just below the hyperechoic epithelial layer may be indicative of an absent Bowman’s layer with concomitant edema.¹⁵ The ability to delineate the zone of endothelial pathology and the presence or absence of iridocorneal adhesions is particularly important given recent advances in endothelial keratoplasty and the potential application of these approaches to appropriate cases of congenital corneal opacification (Figure 8.2).

Figure 8.2 Congenital corneal opacity. Note focal absence of corneal endothelium, Descemet’s membrane and corneal stroma (A). Peter’s anomaly (B). Note abnormal iridocorneal adhesions.

Reproduced with permission from: Heur M, Jeng BH. Anterior segment disorders. Ultrasound Clin 2008; 3(2):201–206.⁵¹

Corneal edema

Some of the characteristic features of corneal epithelial edema – hydropic intra- and extracellular changes and intercellular vesicles – increase the quantity and intensity of echo interfaces and result in the appearance of a thicker, more reflective epithelium and Bowman’s layer. An increase in the thickness and the reflectivity of the stroma also occurs with the increased spacing of corneal lamellae and appearance of large interlamellar vesicles.^2,4

With UBM it is possible to detect the cause of corneal edema in the majority of cases and to plan the correct surgical approach (Figure 8.3).⁴ UBM can provide particularly useful information in cases of corneal edema related to acute hydrops in patients with keratoconus, bullous keratopathy,¹⁶ and total corneal decompensation secondary to iridocorneal touch in iridoschisis (Figure 8.4).¹⁷

Figure 8.3 Corneal edema. Visualization of Descemet’s membrane detachment. Radial scan shows irregularly thickened cornea with a smooth, highly reflective detachment of Descemet’s membrane (arrow).

Reproduced with permission from: Heur M, Jeng BH. Anterior segment disorders. Ultrasound Clin 2008; 3(2):201–206.⁵¹

Figure 8.4 Acute hydrops in keratoconus. Slit lamp photograph showing severe corneal edema with acute hydrops in the left eye (A). Ultrasound biomicroscopic image showing a rupture of Descemet’s membrane and deep cystic intrastromal clefts that were not detected by slit lamp examination (B).

Reproduced with permission from: Nakagawa T, Maeda N, Okazaki N, et al. Ultrasound biomicroscopic examination of acute hydrops in patients with keratoconus. Am J Ophthalmol 2006; 141(6):1134–1136.¹⁶

Descemet’s membrane detachments are a common complication of intraocular surgery that can lead to corneal edema. Although spontaneous reattachment occurs in some cases, edema and visual loss can persist and diagnosis is often difficult at the slit lamp microscope in cases of diffuse edema. UBM can be a useful adjunct in visualizing the membrane for diagnosis and for confirming correct suture placement and membrane repositioning during the repair.^18,19

Corneal dystrophy

Corneal dystrophies typically are diagnosed clinically based on the specific layer of the cornea affected and characteristic appearances on slit lamp biomicroscopy. UBM of granular dystrophy shows highly reflective hyaline deposits in the superficial stroma and correlates well with OCT findings (Figure 8.5).

Figure 8.5 Corneal dystrophy. UBM showing highly reflective hyaline granules in the superficial stroma of cornea with granular dystrophy.

Reproduced with permission from : Pavlin CJ, Foster FS. Ultrasound Biomicroscopy of the Eye, Springer Verlag, New York 1994.

Although UBM may be useful to identify affected regions in the setting of corneal dystrophy, Rapuano has presented data that casts doubt upon the accuracy of central stromal lesion depth measurements with a 50 MHz UBM device.⁷ In 34 eyes undergoing excimer laser phototherapeutic keratectomy (PTK) for a variety of primary or recurrent anterior stromal corneal dystrophies, post-hoc determinations of lesion depth from UBM images did not correlate significantly with the PTK ablation depth.

Corneal biomechanical imaging

A variety of acoustic imaging techniques are being explored as methods of more directly characterizing corneal biomechanical properties and ultimately, ectasia risk (Chapter 19). In 1991, Ophir first described the use of ultrasound speckle tracking during tissue compression for inferring elastic properties – specifically, the elastic modulus – in a non-destructive manner.³² By measuring the displacement of tissue during application of a known deforming force, absolute and relative estimates of local tissue stiffness can be obtained. Hollman et al subsequently extended the concept to porcine cornea (Figure 8.6).³³ More recently, sonic wave velocity measurements^34,35 and supersonic shear imaging³⁶ have been used to demonstrate the stiffening effects of collagen crosslinking, an emerging treatment for keratoconus (Figure 8.7). Advances in this area are likely to lead to more sensitive and specific diagnostic tools for detecting keratoconus, assessing the biomechanical impact of keratorefractive surgery, and monitoring the effects of treatments for ectasia.

Figure 8.6 Conventional ultrasonic backscatter B-scan with a 50 dB grayscale (A, left). Strain image from ultrasound. Black is compressional deformation, and white is expansional deformation (A, right). “Hot” color map of strain in stroma (B, left). “Cool” color map of strain in epithelial and endothelial layers (B, right).

Reproduced with permission from: Hollman KW, Emelianov SY, Neiss JH, et al. Strain imaging of corneal tissue with an ultrasound elasticity microscope. Cornea 2002; 21(1):68–73.³³

Figure 8.7 A corneal surface wave elastometer prototype with emitting and receiving terminals (A). Surface wave velocity measurements across a corneal incision indicating decreased stiffness (B).

Modified with permission from: Dupps WJ, Jr., Netto MV, Herekar S, Krueger RR. Surface wave elastometry of the cornea in porcine and human donor eyes. J Refract Surg 2007; 23(1):66–75.³⁴

Intraocular lens implantation

Intraocular lens (IOL) implantation is the optimal method of correcting aphakia after cataract extraction (Chapter 7). Ideally, the IOL is placed in the normal anatomic lens position, behind the iris plane, with support from the capsular bag. There are some instances, however, when the lens cannot be placed in the bag or the haptics are inadvertently malpositioned (Figure 8.8). UBM has been used to evaluate the position of the IOL optic and haptics after cataract surgery and is particularly helpful in cases of posterior capsule rupture, zonular instability, and determining the position of scleral-fixated IOL haptics relative to the ciliary sulcus (Figure 8.9). UBM is therefore an important tool for planning appropriate intervention and minimizing complications such as hyphema (Figure 8.10), uveitis, corneal decompensation, IOP elevation, lens remnants (Figure 8.11), retinal detachment, lens malposition, and a poor visual outcome.^37–43

Figure 8.8 Posterior chamber IOL. Radial scan of the central iris and posterior chamber IOL shows a slight tilt off the horizontal axis indicating displacement of the posterior chamber IOL (A, arrow). Posterior chamber IOL displaced temporally with the haptic abutting the peripheral iris (B, arrow).

Reproduced with permission from: Heur M, Jeng BH. Anterior segment disorders. Ultrasound Clin 2008; 3(2):201–206.⁵¹

Figure 8.9 Haptic sutured at the sulcus region (A, arrow) and sutured posterior to the pars plicata (B, arrow).

Reproduced with permission from: Manabe S, Oh H, Amino K, Hata N, Yamakawa R. Ultrasound biomicroscopic analysis of posterior chamber intraocular lenses with transscleral sulcus suture. Ophthalmology 2000; 107(12):2172–2178.⁴²

Figure 8.10 Layered hyphema on the posterior corneal surface (arrows) and on the posterior chamber IOL (arrowhead).

Figure 8.11 Lens remnants after cataract surgery. Slit lamp photograph of lens remnant admixed with blood in the inferior capsular bag (A). Retroillumination reveals opacification (B) and UBM confirms thickening of the capsular bag (C). Note that the posterior chamber IOL is not displaced.

In anterior chamber IOL (ACIOL) implantation for aphakia or phakic correction of ametropia, ultrasound techniques are useful for preoperative determination of anterior chamber depth and angle-to-angle diameter to facilitate proper lens sizing and minimize the risk of corneal endothelial decompensation. Postoperative imaging is useful for visualizing the location of the haptics in relation to the iris, iridocorneal angle and ciliary body in cases of suspected malposition⁴⁴ and for directly assessing the distance between the corneal endothelium and ACIOL.⁴⁵ Corneal decompensation secondary to malpositioned ACIOL haptics can progress to the point of requiring a corneal transplant, and in such cases, UBM can be used to determine the extent of adhesions over implant haptics and predict the ease of IOL explantation.⁴⁶

UBM and VHF digital UBM also provide key anatomic dimensions for more optimal sizing of posterior chamber phakic IOL, which rest in the pre-crystalline lens space and are supported by haptics in the ciliary sulcus (Chapter 6).⁴⁷ The postoperative vault between the phakic IOL and the crystalline lens can be evaluated and is thought to be a predictor of anterior cataract formation and pupillary block glaucoma, the two most important complications of such lenses.⁴⁸

Anterior segment trauma

UBM can be used to visualize traumatic lens changes such as focal cataract and zonular dehiscence (Figure 8.12). Iridocorneal angle structures and the ciliary body can also be assessed by UBM in detail allowing for differentiation between iridodialysis (Figure 8.13), angle recession, and cyclodialysis in cases of trauma (Figure 8.14). UBM is of particular importance for diagnosing and evaluating cyclodialysis clefts, even in the presence of a closed angle, allowing for determination of the extent of dialysis and refinement of the surgical plan (Chapter 16).^49,50

Figure 8.12 Lens injury. Focal cataract (A, arrow). The edge of dilated pupil is barely visible (A, arrowhead). Radial scan shows the absence of the zonule normally extending from the ciliary process (B, arrow) to the lens surface (B, arrow).

(Image courtesy of Charles J. Pavlin MD, Toronto, Canada.) Reproduced with permission from: Heur M, Jeng BH. Anterior segment disorders. Ultrasound Clin 2008; 3(2):201–206.⁵¹

Figure 8.13 Iridodialysis. Radial scan shows complete separation of the iris from the root (arrow).

Reproduced with permission from: Heur M, Jeng BH. Anterior segment disorders. Ultrasound Clin 2008; 3(2):201–206.⁵¹

Figure 8.14 Cyclodialysis. Goniophotograph showing cleft in the anterior chamber angle (A, arrows). Radial scan shows complete separation of the ciliary body from the scleral spur (B, asterix).

Reproduced with permission from: Heur M, Jeng BH. Anterior segment disorders. Ultrasound Clin 2008; 3(2):201–206.⁵¹

Anterior segment foreign body

Foreign bodies are localized readily by UBM, and they generate characteristic acoustic artifacts on ultrasonography based on their composition that allow detection of even small foreign bodies through media opacities or in concealed locations such as the iridocorneal angle or behind the iris (Figure 8.15).⁵⁰ Foreign bodies containing pockets of air, such as wood and concrete, create shadowing because of the dampening of the sound waves by air; foreign bodies that are more dense, such as metal and glass, create reflective tails because of internal reflection of the sound waves.

Figure 8.15 Metallic intraocular foreign body. Radial scan shows an irregularly shaped, highly reflective foreign body in the anterior angle (arrow). Note the shadowing of the intraocular structures beneath the hyperechoic foreign body.

Reproduced with permission from: Heur M, Jeng BH. Anterior segment disorders. Ultrasound Clin 2008; 3(2):201–206.⁵¹