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Ординатура / Офтальмология / Английские материалы / Handbook of Pediatric Strabismus and Amblyopia_Wright, Spiegel, Thompson_2006

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42

HANDBOOK OF PEDIATRIC STRABISMUS AND AMBLYOPIA

manipulate these functions surgically to correct specific motility disorders. The Harada–Ito procedure, for example, involves tightening the anterior fibers of the superior oblique tendon. Because the anterior tendon fibers intort the eye, the Harada–Ito procedure can be used to treat extorsion associated with superior oblique palsy.

The trochlear nerve innervates the superior oblique muscle at its midpoint from outside the muscle cone. The superior oblique muscle is, in fact, the only eye muscle innervated on the outer surface of the muscle belly. This unique innervation explains why a retrobulbar anesthetic block results in akinesia of all the eye muscles except the superior oblique muscle.

TROCHLEA

The trochlea (Latin for pulley) is a cartilaginous U-shaped structure attached to the periosteum that overlies the trochlear fossa of the frontal bone in the superior nasal quadrant of the orbit. It has been taught that the superior oblique tendon moves through the trochlea much like a rope through a pulley. Anatomic studies have shown, however, that tendon movement is not that simple. Within the trochlea is a connective tissue capsule with connective tissue bands that unite the superior oblique tendon to the surrounding trochlea (Fig. 2-15).46 Some of the tendon slackening distal to the trochlea may come from a telescoping elongation of the central tendon (Fig. 2-16).19 This telescoping elongation of the tendon appears to be caused by movement of the central tendon fibers that have scant interfiber connections. Thus, the mechanism for tendon movement is complex, with at least two mechanisms: (1) tendon movement through the trochlea (pulley and a rope) and (2) tendon elongation (telescoping).

INFERIOR OBLIQUE MUSCLE

It is the principal extortor of the eye; however, other actions include elevation (secondary) and abduction (tertiary). The inferior oblique muscle originates at the lacrimal fossa located at the anterior aspect of the inferior nasal quadrant of the orbit (see Fig. 2-13). Starting at the lacrimal fossa, the inferior oblique muscle courses posteriorly and temporally underneath the inferior rectus muscle to its scleral insertion, which is adjacent to the inferior border of the lateral rectus muscle (see Fig. 2-14). The inferior oblique muscle has fascial connections to the lower

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A

B

FIGURE 2-15A–B. Histology of the trochlea. (A) Low-magnification cross section of midtrochlea. H&E stain. Note horseshoe shape of cartilaginous tissue and the fibrous connective tissue ring that surrounds the superior oblique muscle. At this cross section, the superior oblique is two-thirds muscle and one-third tendon. (B) High-magnification cross section of superior oblique muscle in midtrochlea shows fibrous connective tissue ring connecting to muscle via fine fascial septae.

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HANDBOOK OF PEDIATRIC STRABISMUS AND AMBLYOPIA

C

D

FIGURE 2-15C–D. (C) Low-magnification cross section of superior oblique tendon exiting the trochlea. Note small area of cartilage and larger ring of fibrous connective tissue that surrounds the superior oblique tendon as the tendon capsule. At this section, the superior oblique is onethird muscle and two-thirds tendon. (D) High magnification of the superior oblique tendon exiting the trochlea. Note the superior oblique tendon capsule consists of circumferential onionskin layers of fibrous connective tissue. The tendon capsule is attached to the superior oblique tendon capsule by circumferential connective tissue fibers. (From Wright et al., Ref. 46, with permission.)

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FIGURE 2-16. Diagram of anatomy of the trochlea. Note the central fibers of the tendon expand and retract more than the peripheral tendon fibers. (From Ref. 19, with permission.)

border of the lateral rectus muscle and to the overlying inferior rectus muscle via Lockwood’s ligament (see Fig. 2-11). When the inferior oblique muscle contracts, it pulls the back of the eye down and in toward the insertion at the lacrimal fossa. This action produces elevation, abduction, and extorsion (Fig. 2-14). Important structures near the inferior oblique insertion include the macula and inferior temporal vortex vein (Fig. 2-14). The inferior oblique muscle has only 1 mm of tendon at its insertion.

The inferior oblique muscle is innervated by the inferior branch of the third nerve at a point just lateral to the inferior rectus muscle. Innervation occurs at the posterior aspect of the inferior oblique muscle belly, and the nerve is accompanied by blood vessels forming a neurovascular bundle. This neurovascular bundle is surrounded by an inelastic capsule of collagen tissue that protects the inferior oblique nerve from damage caused by stretching.39 The neurovascular bundle with its insertion into the posterior aspect of the muscle is an important structure in regard to inferior oblique surgery. Anterior transposition of the inferior oblique muscle is an effective surgical

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HANDBOOK OF PEDIATRIC STRABISMUS AND AMBLYOPIA

procedure used to treat inferior oblique muscle overaction; however, the complication of postoperative limited elevation has been reported.5,25,26,47 This complication is caused by anteriorizing the posterior muscle fibers at, or anterior to, the inferior rectus muscle insertion, because this tightens the inelastic neurovascular bundle.38 The tight neurovascular bundle acts as the functional origin of the inferior oblique muscle and changes the action of the inferior oblique muscle from an elevator to a depressor (Fig. 2-17A).16 This author has coined the term J-deformity for this acute bend of the anteriorized inferior oblique.47 When the patient looks up, the inferior oblique muscle contracts along with the superior rectus muscle, but the anteri-

Inferior oblique

Maxillary bone

muscle

 

Neurofibrovascular

Inferior rectus

bundle

muscle

FIGURE 2-17A,B. (A) Diagram of inferior oblique muscle anteriorization with “J-deformity.” The J-deformity is caused by anterior placement of the posterior inferior oblique muscle fibers to the level of the inferior rectus muscle insertion. Because the neurovascular bundle of the inferior oblique muscle inserts in the posterior muscle belly, anteriorization of the posterior muscle fibers produces a tight neurovascular bundle; this causes limited elevation of the eye as active contraction of the anteriorized inferior oblique muscle pulls against the tight neurovascular bundle.16

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Vortex vein

Inferior oblique muscle

Inferior rectus muscle

FIGURE 2-17A,B. (B) Diagram of the “graded anteriorization” technique described by Guemes and Wright that is effective in reducing inferior oblique overaction but avoids the postoperative complication of limited elevation.16 The new inferior oblique muscle insertion is shown being placed 1 mm behind the inferior rectus muscle insertion, and the posterior muscle fibers are placed an additional 4 to 5 mm further posterior, and parallel to the inferior rectus muscle axis. Note that the posterior placement of the posterior muscle fibers avoids the J-deformity. By keeping the posterior muscle fibers posterior to the anterior fibers and avoiding the J-deformity, the neurovascular bundle remains loose, preventing postoperative limitation of elevation.

orized inferior oblique muscle now depresses the eye and limits elevation; this is an active leash caused by inferior oblique contraction, and forced ductions on patients with this complication of limited elevation often show only slight restriction to supraduction. The complication of limited elevation can be avoided while maintaining excellent results by anterior transposition of the anterior muscle fibers at, or a millimeter or two behind, the inferior rectus insertion. Be sure to keep the posterior fibers back, behind the anterior fibers. Placing the posterior muscle fibers several millimeters posterior to the inferior rectus insertion and in line with the inferior rectus muscle prevents the J-deformity (Fig. 2-17B).16,47

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HANDBOOK OF PEDIATRIC STRABISMUS AND AMBLYOPIA

EXTRAOCULAR MUSCLE HISTOLOGY

As are other skeletal muscles, extraocular muscles are made up of striated fibers that, on electron microscopy, show the typical banding pattern of sarcomeres with overlapping threads of actin and myosin. Also resembling other muscles, the strength of an extraocular muscle contraction is dependent on the number of motor units activated (recruitment) and the frequency of muscle fiber stimulation. Extraocular muscles, however, do show some interesting anatomic and physiological differences from other skeletal muscles. The fibers are variable in size, are considerably smaller, and contract more than 10 times faster than other skeletal muscle. Extraocular muscle fibers are innervated at a high nerve fiber to muscle fiber ratio (almost 1:1), whereas other skeletal muscle can have up to 100 muscle fibers for every nerve fiber. This rich innervation, teamed with a fast muscle reaction time, contributes to the precision, accuracy, and control of eye movements.

Another distinction of extraocular muscles is the presence of two distinct muscle fiber types: fast muscle fibers and slow muscle fibers. The fast, or twitch, fibers are single innervated fibers (SIF), innervated by a large motor neuron with “en plaque” neuromuscular junctions and are typical of mammalian skeletal muscle. The SIF can be classified into three types: red, intermediate, and white. Red SIF have the highest density of mitochondria and are the most fatigue resistant, while the white SIF have fewer mitochondria and are less resistant to fatigue. Intermediate and white fibers provide the high transient force needed for the extremely fast saccadic eye movements.

Slow, or tonic muscle fibers, are multiple innervated fibers (MIF) innervated by small-diameter motor nerves with “en grappe” neuromuscular endings characteristic of avian and amphibian muscles. MIF are thought to participate in smooth pursuit movements and static muscle tone to hold and maintain eye position, and SIF probably also play a supportive role in tonic control of eye position and pursuit eye movements. The exact functions of the variety of specific muscle fiber types are unknown, and it is likely that various fibers have overlapping functions.28

Within extraocular muscle tissue are neuromuscular spindles that are concentrated at the muscle–tendon junction. Neuromuscular spindles are thought to be sensory organs providing information on muscle tone to the brain.9 The exact role

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of the muscle spindles is unknown, but they may provide proprioceptive feedback to motor centers in the brain regarding muscle tone and eye position. Muscle spindles may explain why many adult patients experience transient spatial disorientation after strabismus surgery on the dominant eye.

ARCHITECTURE OF THE EXTRAOCULAR MUSCLES AND PULLEYS

Extraocular muscles have two distinct muscle layers seen on transverse sections (cross section). There is a peripheral layer closest to the orbital wall called the orbital layer (OL) and an inner layer closest to the eye globe called the global layer (GL).33,37 OL muscle fibers contain small-diameter fibers with many mitochondria and abundant vessels, staining dark red by Masson’s trichrome. The GL, in contrast, contains larger fibers with variable numbers of mitochondria and fewer vessels; it stains bright red by Masson’s trichrome. Approximately 90% of GL muscle fibers are fast-twitch SIF, with one-third of the SIF being fatigue-resistant red SIF; 80% of OL muscle fibers are twitch-generating SIF and 20% are MIF.33 In humans, OL muscle fibers do not appear to run the entire course of the muscle and do not insert in sclera, as there is a gradual decline in the OL in the anterior aspect of the muscle.11,28

Elastic fibers connect the OL to a fibromuscular pulley sleeve that surrounds each extraocular muscle close to the muscle insertion (see Muscle Pulleys, following) (Fig. 2-18).11 There are also muscle-to-muscle-fiber junctions (myomyous junctions) within the OL. GL fibers, on the other hand, are continuous from their origin in the orbital apex to their insertion by tendon into sclera.28 Most GL fibers act in saccadic eye movements and function only in the field of action of the muscle whereas OL fibers are active throughout the oculomotor range, providing continuous muscle tone to the pulley system.7 Collins hypothesized that OL muscle fibers might have a role in maintaining fixation whereas GL muscle fibers participate in dynamic eye movements.7 An alternative hypothesis proposed by Demer is that OL muscle fibers actively control pulley position, thereby influencing the rotational force vectors during eye movements.11,28

A

FIGURE 2-18A–C. Masson’s trichrome stain of 10- m-thick transverse section of medial rectus at the level of the pulley ring of a 17-month-old human. (A) Low power shows the overall architecture of the pulley (P) that surrounds the medial rectus muscle. Fibers in the orbital layer (OL) (arrowheads) insert in the pulley, shown at high power in (B). The OL muscle layer takes the form of a C-shape and is on the left, delineated by the large arrows; the global layer (GL) fibers are to the right. OL on the left is shown on the bottom.

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51

B

C

FIGURE 2-18A–C. (B) High-power magnification shows the insertion of the OL into the pulley (taken from the upper left box on A). (C) Highpower magnification of the GL and pulley relationship. The GL does not insert into the surrounding pulley (taken from the middle right box on

A).11,28