Chapter 9 Diagnostic Ophthalmic Ultrasound

Rudolf F. Guthoff, Leanne T. Labriola, Oliver Stachs

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Introduction

Ultrasonography is a pervasive diagnostic tool within medicine. It is used to obtain noninvasive images that can aid in the management of patients in almost all fields of medicine. Ultrasound technology has a unique role in ophthalmology since it can provide quantitative and qualitative assessments of the globe and orbit. Ultrasound images are formed by capturing the reflected acoustic signal from different tissues. These images can provide important details of almost every part of the eye from the anterior cornea and ciliary body to the posterior retina and choroid. This chapter will explain the principles involved in ophthalmic ultrasound as well as provide examples of its use within ophthalmology.

Ultrasound – past and present

In 1880, the Curie brothers first demonstrated that a difference in electric potential could be created by mechanically pressing opposing surfaces of a tourmaline crystal.¹^–⁷ This phenomenon is called the piezoelectric effect. This effect is the basis for ultrasound technology and was first applied in underwater sonar systems during World War II.⁸ During that same era, the medical community also adopted the use of ultrasound technology. Scientists realized the diagnostic potential of this technology when they were able to use acoustic wavelengths to study the consistency of a material without damaging the material itself.

In 1949, Ludwig used ultrasound to detect gallstones in patients. The first publication on the use of ophthalmologic ultrasound appeared in the medical literature in 1956.⁹ By the mid-1970s, ophthalmologists were using ultrasound to determine axial length in a clinical setting. These measurements facilitated calculations of intraocular lens power which led to a revolution in cataract surgery.¹⁰ Further innovations came when Baum and Greenwood introduced their two-dimensional B-mode image to ophthalmology.¹¹ Soon afterwards, Bronson et al.¹² developed a hand-held contact transducer for this type of image acquisition which led to the rapid dissemination of ultrasound devices within ophthalmology clinics. The B-mode images could be used to delineate accurately retinal detachments, vitreous membranes, and choroidal tumors. In the early 1990s, new technology made it possible to image the anterior segment of the eye with devices that captured images at higher frequencies of 35–50 MHz. This improved image resolution four- to fivefold and is still the gold standard for analysis of certain anterior-segment disease such as ciliary body effusions, infiltrates, and tumors.

Examination techniques

The ultrasound examination is performed with the patient in a reclined position. The frequency of the ultrasound cannot pass through air; therefore, a coupling medium is needed to transmit the sound waves from the transducer to the ocular tissues. A common coupling agent is methylcellulose (Fig. 9.1). The coupling agent is applied to the tip of the transducer probe, which is then placed on the patient’s anesthetized cornea.

Fig. 9.1 Ultrasound images simulating the effect of transducer (A) without tissue-coupling agent, (B) with partial tissue-coupling agent, and (C) with a complete coupling agent, such as a gel-like contact substance.

A-mode technique

The A-scan is a linear representation of echo amplitude that is acquired along a single line of sight. Measurements of the ocular tissue can be achieved using the time interval between emission of the acoustic pulse and echo return to calculate the distance of the tissue being imaged. A-scan images should only be obtained through open lids since the eyelid tissue can attenuate the sound waves and decrease the resolution. The pressure applied by the examiner to the transducer tip is especially important when obtaining A-scan measurements. Excessive pressure can deform the cornea, and lead to inaccurate measurements.

B-mode technique

The B-scan is a two-dimensional cross-section image formed by mechanically sweeping the transducer over an angle of 50–60° with the probe oriented in a specific axis. A systematic approach should be used to acquire all images. One method is first to obtain axial scans of the globe by placing the probe in the center of the cornea with the transducer tip oriented toward 12 o’clock in order to image the posterior pole and optic nerve. Next, the transducer can be turned temporally 90° to obtain images through the macula. Finally, radial and transverse images of the globe can be obtained by placing the probe at each clock-hour around the limbus. Radial scans are acquired when the probe is placed perpendicular to the limbus and the transducer tip is oriented toward the cornea. Transverse scans are obtained by turning the probe 90°, orienting the transducer tip parallel to the limbus. The images obtained are the acoustic reflections from the opposing inner surface of the globe.

The reflected sound waves are recorded by the device and can be viewed as a two-dimensional image on the screen (Fig. 9.2). The ocular structures can be examined individually. The cornea is characterized ultrasonographically by two separate acoustic interfaces. The anterior chamber appears planoconvex in cross-section. The iris diaphragm cannot be satisfactorily imaged because of the limited lateral resolution power of the normal B-mode. A clear lens is acoustically empty and appears as an ellipsoid structure in axial sections. Similarly, normal vitreous does not give an acoustic signal; however, the presence of a detached posterior vitreous membrane presents an interface that can be imaged by increasing the amplification of the echo signal. The sclera is the most strongly reflecting structure on ocular ultrasonography.

Fig. 9.2 (A) Cross-sectional echogram through a normal globe. (B) Schematic drawing of the eye: the arrow marks the entrance of the optic nerve.

High-frequency ultrasound technique

High-frequency echograms can be used for ultrasound biomicroscopy (UBM). The shorter wavelengths provide better resolution of the anterior structures of the eye, including the cornea, lens, aqueous (Fig. 9.3), and ciliary body (Fig. 9.4).¹³ High-frequency probes range from 50 to 100 MHz.¹⁴^–¹⁶ The 50-MHz probe provides the best balance between depth and resolution for UBM technique. One limitation of this technique is that the shorter wavelengths, from the higher frequency, have poor depth of penetration. UBM cannot visualize structures deeper than 4 mm from the surface.

Fig. 9.3 The ultrasound biomicroscopy images of the anterior segment in (A) a phakic and (B) a pseudophakic eye with multiple echo of implant surface.

Fig. 9.4 Ultrasound biomicroscopy of the ciliary body.The shorter wavelengths are able to obtain high-resolution images of the anterior structures.

UBM requires immersion of the transducer in a medium to transmit the higher-frequency wavelengths. Saline or methylcellulose can be used as the coupling agent and is held in place over the eye with the use of a custom cup during the examination. UBM is performed through open eyelids in order to obtain a good reflection signal. Images produced by UBM have a resolution of 30–40 µm, which is similar to that seen with a low-power microscope.¹⁷

The cornea is the first structure seen on UBM. The anterior-chamber depth can be measured from the posterior surface of the cornea to the anterior lens pole. The posterior lens pole cannot be imaged by UBM due to its distance from the anterior surface. The iris is seen as a flat uniform echogenic area. The iris and ciliary body converge in the iris recess and insert into the scleral spur. The area under the peripheral iris and above the ciliary processes is defined as the ciliary sulcus. The angle of the eye can be studied in cross-section by orienting the probe in a radial fashion at the limbus. The scleral spur is the most important landmark in the angle on UBM.

Doppler ultrasound

Doppler images are obtained by using frequency shifts from acoustic reflections to measure movements within a tissue and flow conditions within vessels. These frequency shifts can be observed in tissue volumes of less than 10 mm. False color can be added to the images based on ultrasound frequency to distinguish between higher and lower flow states, which aids in the interpretation of the final result (Fig. 9.5).

Fig. 9.5 Cross-sectional ultrasonogram through the posterior pole of the eye: color-coded signals from the central retinal artery (red) and the central retinal vein (blue) are displayed inside the optic nerve.

Ultrasound biometry

Basic physics formulae can be used to calculate the speed of sound as it passes through various ocular tissues. This number can then be used to calculate distance measurements within the eye (Fig. 9.6). In order to obtain accurate measurements, the specific speed of sound of the different intraocular media, such as the lens, aqueous, and vitreous, must be known.¹⁸ These formulae provide precise measurements that can be used to measure intraocular tumors or to deduce the axial length of the globe for intraocular lens power calculations.

Fig. 9.6 (A) Immersion A-scan biometry showing peak amplitudes of the signal reflection. (B) B-scan image with distance measurement captured on a frozen scan. Measurements are obtained by placing the cursor marks on the image and reading the distance between points.

Three-dimensional reconstructions

Real-time three-dimensional (3D) and four-dimensional (4D) images are currently used in some medical specialties, including gynecology, obstetrics, and cardiology, but their use in ophthalmology is limited. 3D ultrasonic images can be produced from a series of scan planes.¹⁹^–²² Silverman et al.²³ characterized the ciliary bodies in rabbits and human subjects using 3D high-resolution ultrasound. In the authors’ laboratory a simple extension of the Ultrasound Biomicroscope Model 840 (Humphrey Instruments, Carl Zeiss Group) and VuMax UBM 35/50 (Sonomed) into a user-friendly 3D ultrasonic imaging system was developed (Figs 9.7 and 9.8).²⁴^–²⁸

Fig. 9.7 Prototype of a handpiece for three-dimensional high-frequency scanning using the VuMax UBM 35/50 (Sonomed).

Fig. 9.8 Clinical pictures of the ciliary body with a pigment cyst (A) through a dilated pupil and (B) with retroillumination. (C) The same eye shown with three-dimensional reconstructed volume with oblique sections.

Ultrasound in intraocular pathology

Changes in the shape of the globe

Phthisis

Phthisis is defined as severe atrophy of the globe associated with hypotony. Phthisis is characterized ultrasonographically by a thickened outer scleral wall. Occasionally, calcification or ossification may be observed (Fig. 9.12). This may be due to degenerative processes and from metaplasia of the retinal pigment epithelium (RPE). In advanced cases of phthisis, the sclera and choroid can represent up to 70% of the total volume of the globe. The degree of thickening of the globe in chronic hypotony can be an indication of impending phthisis, but the precise thickness threshold for phthisis formation is unknown.

Fig. 9.12 Circumscribed calcification in the ocular wall in advanced phthisis bulbi. (A) Echographically we find highly reflective changes in the ocular wall from calcification or ossification of the choroid which casts a shadow on the soft tissue located posteriorly. (B) These strong echoes can be selectively imaged by reducing the amplification. (C) Schematic drawing.

Vitreous

Echographic examination can provide information on vitreous structure which is particularly useful when visualization of the posterior pole is poor due to anterior media opacities. Ultrasonographic findings allow the examiner to differentiate dot-, strand-, and membrane-like reflections (Fig. 9.13). Table 9.1 summarizes the most frequent conditions associated with pathologic changes in the vitreous.

Fig. 9.13 Vitreous opacities. In maximal amplification, small heterogeneous spots can be seen echographically, even though the vitreous appears optically clear (left). They act as dot-like reflectors.

Table 9.1 Clinical conditions with ultrasonographically demonstrable vitreous changes

Vitreous degeneration

Vitreous syneresis can appear as dot-like reflections which can be more pronounced in myopia or senile vitreous. During a symptomatic posterior vitreous detachment, the B-mode echo may demonstrate various stages of vitreous syneresis and may reveal the remaining adhesions of the hyaloid membrane to the retinal surface (Fig. 9.14).

Fig. 9.14 (A) Detached posterior hyaloid membrane imaged as a floating structure of low reflectivity. (B) Schematic drawing.

Asteroid hyalosis

The calcium-containing lipids of asteroid hyalosis are suspended in the vitreous framework and act as distinctive sound reflectors (Fig. 9.15). They can demonstrate the dynamics of vitreous movements.

Fig. 9.15 Asteroid hyalosis. (A) Slit-lamp microscopic photograph of the anterior vitreous space. (B) Histological image of asteroid hyalosis shows the calcium crystals adherent to the vitreous scaffold. (C) B-scan cross-section of the crystals, which represent good reflectors for the ultrasound. There is always an echo-free retrovitreal space seen near the ocular walls. (D) Schematic drawing.

Synchysis scintillans

In synchysis scintillans the vitreous is filled with cholesterol crystals. Unlike asteroid hyalosis, these crystals are not suspended within the vitreous but instead float freely in the vitreous space. When the globe moves, the crystals appear in the center of the vitreous body. This clinical picture may resemble asteroid hyalosis, but after a few seconds the cholesterol crystals will sink toward the bottom of the cavity. A-mode images display characteristic flickering spikes from the reflections of these crystals.

Persistent and hyperplastic primary vitreous

The primary vitreous contains the tunica vasculosa lentis, which is part of the fetal vasculature system. During development, the tunica vasculosa lentis emanates from the optic nerve head and supplies the posterior lens. This structure should involute prior to birth. Failure of the primary vitreous to regress fully is termed persistent hyperplastic primary vitreous. As mentioned earlier, this can be associated with microphthalmos and cataract formation in the newborn. The condition persistent hyperplastic primary vitreous can be ultrasonographically characterized by two features. The first is a strand of membrane that extends between the posterior surface of the lens and the area of the optic nerve head. The second is the reduced axial length of the globe from microphthalmos on ultrasound biometry (Fig. 9.16). If the anomaly is only mild, the lens may be clear at birth but may become cataractous when the posterior lens capsule ruptures.

Fig. 9.16 (A–D) Posterior polar cataract in persistent hyperplastic primary vitreous (PHPV). An ultrasonographically demonstrable strand attached to the posterior lens pole points is suspicious for PHPV (A). Frontal plane taken temporally with maximal adduction of the globe (C). (B,D) Schematic drawings. The dark, hatched parts correspond to the opaque area of the posterior cortex and posterior capsule in a child with severe PHPV. (E) Histological section of PHPV as seen at optic nerve head with loupe magnification.

Vitreous hemorrhages

An acute vitreous hemorrhage is an important indication for ultrasonography. Acute hemorrhages can fill the vitreous cavity with small opacities from the particles of the red blood cells. These opacities usually accumulate after a few hours in the lower circumference of the vitreous base (Fig. 9.17).

Fig. 9.17 (A) Conspicuous bleeding into syneretic vitreous; erythrocytes within the vitreous create reflective opacities. A static picture may give the impression of a solid lesion. (B) After a few hours the opacities usually accumulate in the lower aspect of the vitreous cavity. (C) Schematic drawing.

If a detachment of the posterior hyaloid membrane precedes a vitreous hemorrhage, the erythrocytes frequently precipitate on to a vitreous strand (Fig. 9.18). This strand may be responsible for the development of a retinal tear, and its traction can be demonstrated directly in acoustic sectioning (Fig. 9.19). A circumscribed thickening of the ocular wall in cross-section may indicate the presence of a retinal operculum (Fig. 9.20). This area should be localized echographically and then carefully scrutinized with ophthalmoscopy if possible.

Fig. 9.18 Fresh vitreous hemorrhage. In a cross-sectional echogram the vitreous framework converges towards the ocular wall. Blood precipitates increase the acoustic reflectivity of the vitreous. Traction has to be assumed where the vitreous is in contact with the ocular wall.

Fig. 9.19 (A) Recent vitreous hemorrhage. The low reflecting membranes float freely with ocular movement. A newly formed horseshoe tear may be present at their connection point to the wall. (B) Schematic drawing.

Fig. 9.20 (A,B) Recent vitreous hemorrhage. Erythrocytes have precipitated on to the partly detached posterior hyaloid membrane, increasing its acoustic reflectivity. (C) Schematic drawing.

In larger hemorrhages, the blood can also disseminate into multiple pre-existing vitreous compartments. In the early phase of this process, the erythrocytes will collect in the retrovitreal space (Fig. 9.21). The retrovitreal space may completely clear after a few days or weeks due to its high fluid exchange rate; however, blood on the vitreous framework absorbs much more slowly (Fig. 9.22).

Fig. 9.21 (A) Vitreous hemorrhage with posterior vitreous detachment emphasizing the retrovitreal space. (B) In the early stage after the hemorrhage, erythrocytes accumulate in the retrovitreal space. They may ensheath the part of the vitreous that was free of blood and had a normal structure. (C) Schematic drawing.

Fig. 9.22 The retrovitreal space may completely clear after a few days or weeks due to its high fluid exchange rate; however, blood on the vitreous framework or located subretinally absorbs much more slowly (A). (B) Schematic drawing.

Vitreous hemorrhage from neovascularization

Hemorrhages that develop from proliferative changes in patients with diabetic retinopathy and retinal neovascularization will always be accompanied by pathologic changes in the vitreous. Vitreous membranes tent rectilinearly between the adhesions to the retina. The normal aftermovements that should occur in the vitreous after eye movements are extinguished in the presence of peripheral neovascular tufts. The vitreous tufts create adhesions that encircle the posterior pole. This is an ominous sign, which is indicative of early retinal tractional detachment from these circular adhesions (Fig. 9.23). Choroidal neovascularization from age-related macular degeneration will have hemorrhage in multiple layers of the eye (Fig. 9.24).

Fig. 9.23 (A) Beginning traction detachment at the posterior pole with vitreous contraction and proliferative diabetic retinopathy, which is hidden behind a diffuse vitreous hemorrhage. A springboard-like, taut, detached hyaloid membrane is still adherent to the retina at the posterior pole and has led to a traction detachment in several places. (B) Schematic drawing.

Fig. 9.24 (A) Extensive vitreous hemorrhage from disciform macular degeneration. The blood dissipates into the preretinal or intrachoroidal space, into the area of the macular lesion and into the detached vitreous. The retrovitreal space is echo-free because of its high fluid exchange. (B) Schematic drawing.

Terson syndrome

Terson’s sign is a multilayered, intraocular hemorrhage at the posterior pole that typically occurs after blunt trauma to the head. This is usually accompanied by a subarachnoid hemorrhage. If the posterior hyaloid membrane is still attached, the preretinal bleeding will slowly diffuse into the formed vitreous (Fig. 9.25). This can damage the underlying retina and may be an indication for an early vitrectomy.

Fig. 9.25 (A,B) Retrovitreal bleeding associated with a subarachnoid hemorrhage (Terson syndrome). The bleeding originates from the area of the optic nerve head. (C) Schematic drawing.

Intraocular infections

Ocular infection that extends toward the anterior segment or results in a hypopyon formation will have changes within the anterior vitreous space that are demonstrable on ultrasound. A thickening of the retina or choroid can be seen if the inflammation penetrates to the outer layers of the globe (Fig. 9.26). After only a few hours, these changes may involve the entire vitreous body (Fig. 9.27). If panophthalmitis follows a perforating injury, ultrasound evaluation can detect a local reaction at the entrance point of the infection (Figs 9.28 and 9.29).

Fig. 9.26 (A,B) Panophthalmitis after an intraocular operation. Widening of the ocular wall to about 2.1 mm indicates inflammatory choroidal infiltrates. (C) Schematic drawing.

Fig. 9.27 Vitreous abscess that caused a bacterial orbital inflammation. (A) B-scan ultrasonography demonstrates a highly reflective vitreous body which is partly detached from the retina. (B) Schematic drawing of this image. (C) Posterior pole shows infiltration of Tenon’s space and widening of the optic nerve sheath. (D) Schematic drawing.

Fig. 9.28 Posttraumatic intraocular infection starting from the side of perforation. (A) B-scan ultrasonography demonstrates localized thickening of the ocular wall indicating the side of the perforation. The vitreous is filled with inflammatory cells, the posterior hyaloid is thickened, and there is a localized retinal detachment. (B) Schematic drawing.

Fig. 9.29 Chronic inflammation with massive vitreous infiltration after pars plana vitrectomy and scleral buckle. (A) Remnants of the infiltrated vitreous can be seen at the vitreous base anterior to the scleral buckle. (B,C) Cross-sections through the vitreous base. (D) Schematic drawing.

Vitreous inflammation

Inflammatory and hemorrhagic vitreous changes cannot be differentiated on the basis of ultrasonographic findings alone. Both conditions may cause densification of pre-existing vitreous structures with subsequent shrinkage of the vitreous; tractional detachment of the retina can occur, especially if there are postinflammatory adhesions between the vitreous and retina. In chronic uveitis, an early and complete posterior vitreous detachment can occur and cause the formed vitreous to shrink and form a frontal membrane that extends across the vitreous base (Fig. 9.30). If this membrane adheres to the ciliary body, it may detach the ciliary body and produce subsequent ocular hypotony.²⁹

Fig. 9.30 Phthisis oculi in chronic panuveitis. (A) The vitreous has shrunk to form a frontal membrane of high acoustic reflectivity. The ocular wall is widened to 2.9 mm. (B) Using linear amplification, the various layers of the ocular wall have become clearly outlined. (C) Isolated areas of the ocular wall show high acoustic reflectivity, which indicates calcification of the choroid or in the sclera. (D) Schematic drawing highlighting wall thickness.

Intraocular foreign bodies

Intraocular foreign bodies induce a change in echo reflectivity which is based on the composition of the material (Figs 9.31–9.33). The change in the reflectivity on the image should be a helpful clue in the localization of the foreign body within the globe; however, this is not always the case since the foreign bodies can also create signal artifact on echograms that can make identifying their exact location difficult. For example, large metallic foreign bodies have significant artifacts from strong reflected signals that can distort their true location. In addition, foreign bodies from trauma can be associated with air bubbles within the vitreous that can mask the presence of the nearby foreign body within the acoustic shadow (Fig. 9.34).

Fig. 9.31 (A) Metallic foreign body in the vitreous with total retinal detachment. (B) The foreign-body spike is characterized by its high amplitude and repetitive echoes. (C) With reduced sensitivity the foreign body can almost be imaged as an isolated echo.

Fig. 9.32 Acute perforating injury with intraocular metallic foreign body. (A) Ultrasonographically, there is a typical foreign-body echo with repetitive spikes in the vitreous about 2 mm in front of the ocular wall. (B) Decreasing the amplification displays the foreign-body echo as the only intraocular structure remaining visible on ultrasonography. (C) Schematic drawing.

Fig. 9.33 (A) Intraocular foreign body of a piece of wire. (B) The anterior end of the wire remained visible in the lens. Cross-sectional image taken temporally with maximal adduction of the globe. (C) Frontal section through iris and lens. (D) Schematic drawing.

Fig. 9.34 Computed tomography image of a metallic foreign body wedged into the ocular wall with an air bubble adjacent to it.

Retina

Ultrasound can be used to assess the structure of the retina in order to discern anatomical changes such as retinal tears and detachments. It can also be used to identify changes in retinal thickness from infiltrative or exudative ocular diseases. The sound reflections in ultrasound images can delineate these pathological retinal changes even in eyes with opaque anterior media. This is a particularly useful tool since many diseases that affect the retina can also lead to vitreous changes that limit direct visualization. It is important to have a strong fundamental knowledge of ocular anatomy as well as a good technical approach for acquiring ultrasound images in order to make accurate assessments of retinal disease on ultrasound. This section will review the anatomical features of common retinal conditions as well as the special techniques needed to examine the retina with ultrasound.

Acute retinal detachment

In a retinal detachment, the neurosensory retina separates from the RPE layer. This development allows fluid to collect in the potential space between these two layers. The detached neurosensory retina appears as a membrane in the vitreous space on ultrasound. Partial retinal detachments may still maintain connections to the optic nerve or ora serrata since these areas have the strongest connections to the retina. Identification of these connections on ultrasound can distinguish a partial retinal detachment from a vitreous or choroidal detachment, which would have different anatomical connections (Fig. 9.35). A complete retinal detachment can form a funnel shape due to the retina folding in the center of the globe.

Fig. 9.35 (A) Complete retinal detachment extending between the optic nerve head and the ora serrata. Heterogeneous material in the anterior vitreous is a sign of vitreous reaction. (B) Schematic drawing.

Complicated retinal detachments with severe pathology can make it difficult to identify all the structures on ultrasound (Fig. 9.36). For example, in severe trauma cases that are associated with proliferative vitreoretinopathy or in advanced diabetic disease associated with proliferative retinopathy, the membranes formed within the vitreous can appear similar to a true retinal detachment. The following questions can guide the ultrasound examination of the retina in order to differentiate these common causes of vitreous membranes:

• What is the spatial extent of the membrane? At which point is there contact with the ocular wall?

• What is the shape of a cross-section of the membrane, especially in the optic nerve head area?

• Which aftermovements occur?

• How great is the difference of the spike from the membrane in question to the scleral standard or to the echo from a standard reflector?