Diagnostic pathway. Diagnostic pathway and classification of extraocular muscle dysfunction in pediatric patients with oculoplastic disorders
The above classification of associated extraocular muscle dysfunction can assist with a diagnosis of lid or orbital disorders, such as paralytic strabismus associated with ptosis in cranial nerve disease and restrictive strabismus associated with proptosis or lid retraction in thyroid ophthalmopathy. Neuropathic or myopathic processes may first present as orbital or lid abnormalities and only later, or on careful examination, reveal associated extraocular muscle dysfunction.
Separate examination of both sensory and motor systems in children with lid and orbital disease is necessary for accurate diagnosis and treatments. A routine examination of the visual sensory system and ocular motor system should be part of the initial and subsequent ophthalmic evaluation in children with lid and orbital pathology.
Education of patients and families regarding associated extraocular muscle dysfunction , its clinical consequences, and probable treatments is necessary for complete care in these children. Staging of medical and surgical treatments requires cooperation between the various ophthalmic subspecialists involved in the care of these patients.
To understand the pathophysiologic relationship in children between lid and orbital disorders and extraocular muscle dysfunction, an appreciation of developmental anatomy is needed. Embryologic development of the mesenchymal process destined to become the extraocular muscles is intimately related to the development of neighboring structures. The developing extraocular muscle complexes arise simultaneously with and are connected to important lid and orbital structures [9–12]. The superior extraocular muscle complex begins as a condensation of mesenchyme in the superior orbit at the 5-mm stage of gestation . The persistence of some embryologic attachments between the superior rectus and levator muscles after full development is evident as attachments between the horn of the levator aponeurosis and the superior rectus. A more permanent anatomic relationship exists between the inferior orbital extraocular muscles and the muscles of the lower lid (Fig. 11.2). The lower lid retractors, inferior rectus, and inferior oblique muscle join to form a condensation of tissues that is the central part of Lockwood’s ligament. Surgery on either the lower lid retractors or the inferior rectus alone may result in a malposition of the other with resulting strabismus or lid malposition.
Cadaveric orbital dissection. Cadaveric orbital dissection illustrating the anatomic relationship of the lower lid retractors, head of the capsulo-palpebral fascia, and the inferior rectus
Developmental anomalies of the orbits (microphthalmia, anophthalmia, orbital hypoplasia, and retrusion), especially those occurring with major craniofacial malformations, often have associated abnormalities of extraocular muscle function [14–19]. This may be due to associated primary maldevelopment of the muscles and tendons or a secondary effect of abnormal supporting orbital structures [1–3, 18, 19]. Perimuscular orbital structures allow for smooth coordinated movements of the extraocular muscles. Lid movements have voluntary and involuntary static and dynamic functions. The relative positions of the lids to the eye are held constant due to complex neuromechanical control mechanisms. Interruptions of normal lid and orbital functional interrelationships can be due to many mechanisms from disturbances at the level of the central nervous system to the extraocular muscles alone.
Classification of Strabismus and Oculoplastic Disorders
Strabismus and extraocular muscle dysfunction in the pediatric population most often occurs without any associated disorders of the lids and orbits. When strabismus does occur in association with pediatric oculoplastic disorders, it can be classified as that which is directly due to the oculoplastic disorder (secondary strabismus), that which causes the oculoplastic disorder (primary strabismus), and that which occurs simultaneously and has no etiologic connection to the oculoplastic disorder (associated strabismus) (Fig. 11.1).
Secondary Strabismus Types
These disorders of extraocular muscle dysfunction are directly due to disturbances of the orbits, lid, and adnexa. Anomalous development of the lids and orbits occurs frequently with craniofacial disorders and genetic syndromes [1, 4, 16–19]. The major craniofacial anomalies include craniosynostoses and clefting syndromes (see Chap. 38). Extraocular muscle disorders occur very commonly in these patients and are due to both supranuclear and infranuclear abnormalities in the ocular motor system [16–20]. Typical childhood strabismus syndromes, such as infantile esotropia and exotropia, accommodative esotropia, and incomitant strabismus, can occur alone or in combination with absent and maldeveloped extraocular muscles. Genetic syndromes and chromosomal abnormalities are frequently associated with strabismus and extraocular muscle dysfunction.
Trauma is very common in childhood and is a major etiology of visual system damage in children . Extraocular muscle dysfunction is secondary to related damage involving surrounding orbital bones and sinuses. These include soft tissue or muscle entrapment, nerve damage, or secondary restrictive strabismus associated with orbital hemorrhage and scarring. Lastly, bony damage can result in displacement of the orbit with secondary misalignment of the visual axis.
Inflammatory disorders of the orbit commonly result in secondary extraocular muscle dysfunction . The most common orbital inflammations in childhood include infectious cellulitis, idiopathic orbital pseudotumor or myositis, and those orbital tumors with some associated inflammation (rhabdomyosarcoma, capillary and cavernous hemangiomas, lymphangioma, and blood dyscrasia) [22, 25]. Orbital infiltrative processes result in a clinical picture of extraocular muscle dysfunction consistent with intranuclear or incomitant strabismus due to changes in the contractility (strength) or length-tension characteristics (stiffness) of the muscles. This results from a combination of factors, such as stretching from proptosis and direct extraocular muscle or nerve infiltration with cells, edema, abnormal extracellular matrix, or tumor tissue.
Many primary extraocular muscle disorders in childhood have secondary orbital and/or lid anomalies. Anomalous development of the extraocular muscles can be due to intrauterine toxins, infections, and chromosomal disorders [9–13]. The incidence of developmental malformations in general is reported to be between 2% and 4% at birth [22, 23]. However, the incidence rises to 6% or 7% if abnormalities that manifest later in life are included [22, 23]. Severe developmental abnormalities of the orbit such as anophthalmos, microphthalmos, cryptophthalmos, craniostenoses, and clefting syndromes have both primary and secondary abnormalities of the extraocular muscle and orbits and are discussed more fully in Chap. 5 [10, 29, 30].
Primary hypoplasia and dysplasia of the extraocular muscles are often associated with abnormalities of the levator and lid retractor muscles, resulting in congenital lid malpositions (ptosis, entropion, ectropion, etc.) (Fig. 11.3). These abnormalities of the orbital extraocular muscles can be associated with canthal dystopia and epicanthal skin abnormalities (Fig. 11.4). Severe forms of congenital dysplasia of the extraocular muscles such as the fibrosis syndromes result in severe associated orbital and lid deformations (Fig. 11.5) .
Unilateral ptosis and strabismus. Patient with congenital unilateral ptosis and combination restrictive/paralytic strabismus due to congenital unilateral complete third cranial nerve palsy associated with hemiatrophy of the ipsilateral brain stem
Primary hypertelorism . Patient with primary hypertelorism displaying numerous canthal disturbances and strabismus
Unilateral fibrosis syndrome . Patient with left congenital unilateral fibrosis syndrome with restrictive strabismus, ptosis, lid lag, and lagophthalmos
Trauma resulting in disorders of the extraocular muscle function is mainly due to interruption of infranuclear oculomotor pathways. This can occur in the central nervous system (brain stem, interpeduncular space), the cavernous sinus, or orbit. Classification of traumatic disorders is the same as elsewhere in the body (e.g., blunt vs. sharp, penetrating vs. nonpenetrating). Traumatic disruption of extraocular muscle function in infancy and childhood is often associated with lid and orbital involvement [9, 12]. The high incidence of associated involvement of these structures has unique implications in this age group [11, 25, 26]. Acquired strabismus, ptosis, and orbital deformities interrupt the normal developmental physiology of vision, including binocularity, refractive development, and orbital growth . This results in amblyopia, persistent loss of binocularity, and continued cosmetic and functional asymmetries in the lids and orbits. The evaluation of trauma in the child is often very difficult, and a complete examination is difficult and can be accomplished only under anesthesia. The potential long-term functional and cosmetic implications of extraocular muscle, lid, and orbital trauma in the pediatric patient require prompt diagnosis and treatment with reversal of amblyogenic factors and restoration of anatomy and symmetry.
Primary inflammatory disorders of the extraocular muscles occur commonly in the pediatric population and often present with a clinical picture due to associated orbital inflammation. Division into infectious and noninfectious inflammatory disorders is important for treatment and prognosis. Infectious myositis is usually associated with contiguous orbital cellulitis but can occur in isolation due to metastatic septic emboli. Noninfectious myositis is usually part of the spectrum of orbital inflammatory pseudotumor, although Graves’s thyroid orbitopathy can also present in childhood. In children, infectious vs. noninfectious myositis and/or orbital cellulitis are often difficult to distinguish clinically because both can present with fever, lethargy, lid and orbital edema, proptosis, orbital pain, and headache. A more complete physical exam (including temperature, ear, nose, and throat, with associated laboratory studies such as complete blood cell count, erythrocyte sedimentation rate, etc. as well as radiologic testing such as computer-assisted tomography [CT] scan and magnetic resonance imaging [MRI]) is needed to differentiate these processes.
Tumors involving the extraocular muscles in infants and children are rare. In a study of computed tomography features of nonthyroid extraocular muscle enlargement, primary or locally invasive neoplasms accounted for 26% of all cases, and 20% of cases were attributable to metastases . Rhabdomyosarcoma and hematologic malignancies are the most common primary neoplasias that involve extraocular muscles. Numerous primary and secondary orbital tumors in childhood (discussed in Chaps. 23 and 24) can invade the extraocular muscles. Regardless of the tumor type, position, or size, the resultant interference with extraocular muscle function clinically appears as either restrictive or paralytic strabismus or a combination of these two forms.
Examination techniques are the most important part of strabismic diagnosis, whether occurring primarily or associated with lid and orbital disorders. The general examination of binocular and extraocular muscle systems involves both sensory (afferent) and motor (efferent) systems. Sensory system examination includes measurement of central visual acuity, fusion, and stereopsis. Like many subjective tests in the pediatric population, accuracy and consistency can be a problem clinically. Vision and visual acuity measurement are discussed fully in Chap. 10. Worth 4-dot testing provides information regarding the child’s binocular status and, if there is a deviation, whether the child is able to alternately suppress either eye. A test of “fine” fusion or stereopsis using stereograms such as Titmus Fly and Random Dot is also given prior to the motor examination to assess the presence of stereopsis in the visual cortex. Although a primary absence or malfunction of cortical fusion may be responsible for many forms of childhood strabismus, disruption of the extraocular muscle system due to orbital disease in infancy can interfere with full development and potential of cortical fusion [28, 29].
Measurement of the ocular deviation is important for several reasons. Accurate measurement of the angle of strabismus in all positions of gaze is an important step in diagnosis of ocular motor system dysfunction. If the deviation is comitant, then dysfunction is likely due to disease above (supranuclear) the level of the ocular motor nuclei (e.g., infantile esotropia). If the strabismic deviation is incomitant, then this is most likely due to disease at or below the level of the ocular motor nuclei (infranuclear), for example, sixth cranial nerve palsy.
Cover–uncover testing, alternate cover testing, and simultaneous prism/cover testing are the standard clinical tests for determining a tropia, tropia plus phoria, and total tropic deviation, respectively. If possible, this should be determined in primary, secondary, and tertiary (oblique) positions of gaze at distance and near with best corrected acuity to an accommodative target. Recording this information in a standard diagram is often helpful for future reference and clinical decision-making (Fig. 11.6).
Ocular motility examination diagram. Ocular motility examination diagram with spaces for recording the patient’s versions and deviation in primary, secondary, and near deviations
If the deviation is incomitant, which is likely in those situations in which one eye has a weak or restricted muscle, then these differences along with clinical versions (ocular rotations with both eyes open) and ductions (ocular rotations with one eye covered) testing are noted. There are many ways of recording versions and ductions. We prefer to use a scale of −4 to +4, with 0 being normal. A −4 version would be a lack of rotation to midline horizontally or vertically with both eyes open (Fig. 11.7). If a restriction is suspected, intraocular pressure in the limited field of gaze may be increased.
Ocular motility examination diagram. Ocular motility examination diagram illustrating recording of a patient with paralytic strabismus due to a right sixth nerve palsy
Special testing is available and is often helpful in diagnosis and quantification of strabismus associated with oculoplastic disorders. These tests may be difficult to perform on infants and young children, although older children are usually compliant. These special tests include forced ductions, forced generations, diplopic fields, and electrooculography. Forced duction and forced generation testing are clinical adjuncts useful in differentiating a “weakness” from a restriction. After instillation of topical anesthetic, the patient is asked to move the eye in the affected direction (Fig. 11.8). The examiner then attempts to manually move the eye further in the same direction. Resistance to further movement of the eye is considered a positive forced duction and is indicative of restrictive disease. When performing forced generation, the eye is grasped at the limbus anterior to the muscle insertion affected; then the patient is asked to move the eye in the field of action of the muscle, while the tester attempts to hold the eye against the patient’s movements (Fig. 11.9). In this way the examiner can “feel” the force generated by voluntary innervation of this muscle. The information obtained after performing these two clinical maneuvers is important for both diagnosis and treatment since approach to treatment of paralytic versus restrictive strabismus is quite different.
Intraoperative forced duction of an inferior restriction. The eye is grasped at the inferior limbus and the globe is gently pulled out of the orbit and rotated superiorly
A forced generation test. A forced generation test can be performed in the office with a cotton tip applicator after anesthetizing the eye and holding it against attempted movements in the field of decreased duction, as in this patient with a right sixth nerve palsy
In patients who complain of diplopia, quantification of their field of single binocular vision (SBV) is important preoperative information. In general, oculoplastic disorders associated with extraocular muscle dysfunction leading to diplopia can be effectively treated. Surgical or medical treatment results in either restoring some SBV or expanding the patient’s field of SBV, but often do not return their field to 100% normal. The diplopic field can be evaluated using the Goldmann perimeter where the patient is placed in the perimeter with the head straight and both eyes open. The examiner’s view places the bridge of the patient’s nose in the patient’s viewing circle by appropriately positioning the chin rest (Fig. 11.10). Isopters are determined dynamically using a target of threshold size and width (e.g., I2c, I4e). The target is presented first centrally or within the center of the patient’s field of SBV. The target is then moved along each meridian until the patient reports edge blurring or frank diplopia. This is marked on a standard perimetric data collection sheet outlined with the normal field of SBV (Fig. 11.11).
Child placed in Goldmann perimeter . Child placed binocularly with the forehead in the middle of the viewing aperture of the Goldmann perimeter in preparation for determination of her field of singular binocular vision
Tester’s view of Goldmann perimetric binocular field measurement. Also displayed is a previously marked normal field of single binocular vision
Imaging techniques are often used when evaluating lid, orbital, and adnexal disease. If the patient has associated extraocular muscle dysfunction, additional diagnostic information can be simultaneously obtained. In addition to obvious structural disease of the extraocular muscles, CT scans and MRI can now be used to assess dynamic function by incorporating cinematic effects. These dynamic imaging techniques can be performed on infants and children and assist with diagnosis of muscle position, weakness, or restriction. Additionally, electrooculography, a noninvasive method of analysis of both the supranuclear and infranuclear ocular motor systems can be utilized. This apparatus uses infrared light to detect motion of the eyes from which an electric signal is generated and analyzed via chart recorders or computer software programs (Fig. 11.12). With oculography a definite diagnosis of restriction versus paresis and quantification of amount of muscle function can be accomplished (Fig. 11.13).
Infrared oculographic goggles. Child with infrared oculographic goggles in position for recording
Oculographic recording. Oculographic recording showing normal conjugate, symmetric horizontal and vertical saccadic activity. Seconds on Y axis. XL = OS horizontal, XR = OD horizontal with rightward and leftward deflections for this axis representing rightward and leftward movements, respectively. YL = OS vertical and YR = OD vertical with rightward and leftward deflections representing upward and downward movements, respectively
Laboratory studies evaluating blood and biopsied tissue are helpful in diagnosis of those oculoplastic disorders associated with systemic diseases and atypical clinical presentations. They are most helpful in diagnosing infections, autoimmune inflammations, and tumors. Testing can broadly be defined as screening tests, such as complete blood cell count, erythrocyte sedimentation rate, antinuclear antibody test, or specific tests, such as cultures and histopathology.
In general, treatment of extraocular muscle abnormalities associated with oculoplastic disorders requires accurate diagnosis and cooperation with planned oculoplastic intervention. The two categories of treatment are medical and surgical. Medical treatments include those topical and systemic agents used to treat the primary etiology, for example, antimicrobials, anti-inflammatories, and antineoplastics. These treatments take precedence over surgical treatment, because they may alone result in effective elimination of the extraocular muscle dysfunction. Other medical treatments of extraocular muscle dysfunction involve spectacles, botulinum toxin, and occasionally topical drops. Spectacles with and without prisms can treat associated refractive errors and diplopia. Botulinum may restore ocular muscle balance by temporally paralyzing muscles antagonistic to those with acquired paresis or restriction [30–37]. This prevents contracture of the antagonist muscle during recovery of nerve function in the affected muscle with a greater chance of restoration of extraocular muscle balance after recovery. Topical drops, such as anticholinesterases, may help with esotropic deviations which are greater at near than distance.