PART two

Introduction to Neuromuscular Anomalies of the CHAPTER 8

Classification of Neuromuscular Anomalies of the Eyes

deviation of the visual axes relative to each in controlling a large esodeviation that becomes Aother is the most common sign in all neuro- manifest when fusion is disrupted with the translu- muscular anomalies of the eyes except for supra- cent occluder of Spielmann.21 nuclear affections. All neuromuscular anomalies In the absence of a properly functioning fusion of the eyes therefore are classified primarily on mechanism, a more or less obvious deviation of the basis of the properties and characteristics of one of the visual lines will be present. Such devia- the deviation, its direction, origin, temporal behav- tions, termed heterotropias, are manifest devia- ior, and various modifications imposed on it by tions not kept in check by fusion. The term hetero- the sensory system. phoria and related terms were formed from the Greek words heteros, ‘‘other,’’ ‘‘different from,’’ and phora, ‘‘bringing,’’ ‘‘carrying’’ (compare and pherein, to bear, carry, a word from which so Heterotropia many medical and scientific words have been coined).19 Phora does not mean a tendency, even Proper alignment of the eyes is guaranteed by a less so the word phoro from which Stevens states normally functioning sensory and motor fusion he derived his term. Stevens’ original definition mechanism. If sensory fusion is artificially sus- of ‘‘heterophoria as a tendency of the visual lines pended by excluding one from participating to turn away from parallelism,’’ copied to this in vision, motor fusion is ‘‘frustrated,’’ as Cha- day in many texts, does not properly describe the vasse4 put it, and a measurable relative deviation phenomenon, as Lancaster11 pointed out. of the visual axes will appear in most patients. In accordance with the foregoing definitions, When the obstacle to sensory fusion is removed, all neuromuscular anomalies of the eyes can be motor fusion in most patients will return the visual separated into two main classes: latent deviations axes to their proper relative positions. The relative () and manifest deviations (hetero- deviations thus elicited are called heterophorias,a tropias). Manifest deviations are known also by very useful term introduced by Stevens.23 Since the generic name of ,orsquint. heterophorias become evident only when normal According to Hirschberg8 the word strabismus cooperation of the eyes is disrupted, they may be originates from the Greek. Hippocrates used the defined as deviations kept latent by the fusion word streblos, ‘‘turned,’’ ‘‘twisted,’’ when he mechanism. Figure 8–1 shows the effect of fusion talked about strabismic subjects and the word is 127 128 Introduction to Neuromuscular Anomalies of the Eyes

position of rest of the eyes.1, 2 This is an unfortu- nate term because ocular muscles are never ‘‘at rest’’ in a living, conscious person. It is known today from electromyographic evidence (see Chapter 6) that electrical activity is continuous in when the eyes are steadily fixating. Indeed, even when fusion is interrupted, the deviation of the visual axes is not a passive but an active process, as shown by the increment and corresponding decrement in electrical activity of certain extraocular muscles. Long before elec- trophysiologic evidence became available, it was obvious that the eyes are never truly at rest in a waking person. Maintenance of the primary posi- tion, fixation, and proper alignment of the visual axes all require the presence of an actively sup- ported tonus and a continuous shift in tonus of extraocular muscles (see p. 111). A differentiation was made therefore between the relative, func- tional, or physiologic position of rest assumed by the eyes when fusion was suspended and the absolute position of rest assumed by the eyes in death before the onset of rigor mortis,15 and in deep anesthesia. The absolute position of rest has also been termed anatomical or static because it is determined solely by anatomical and other mechanical factors.7, 10, 11 Spielmann22 introduced the term fixation-free position to describe the posi- tion of the eyes in the dark or when both eyes are FIGURE 8–1. Manifestation of after disruption covered with semiopaque occluders. This position of fusion with a translucent occluder. is identical to what Lancaster11 called, less descrip- tively, the static position. derived from the verb strephein, ‘‘to twist,’’ ‘‘to The term relative position of rest is an unneces- turn.’’14 The Romans simply adopted the term sary one. Since and fusion are not strabismus into their language from whence it active when the vision of one eye is obstructed, it entered medical terminology. The proper Latin is best to say the particular position that the eyes expressions were paetus and luscus which origi- assume under those conditions is the fusion-free 9 nally meant ‘‘one-eyed.’’ Neither of these terms position. Synonymous terms are the heterophoric 4 or their derivatives are used in English but luscus position and the dissociated position. survived in the French verb loucher, ‘‘to squint.’’ The absolute or anatomical position of the eyes Whether the name of the famous Greek historian in death is generally one of slight divergence and 4, 7, 16 and geographer Strabo (‘‘the squinter,’’ 66 BC–AD elevation, yet it does not attain the divergent 24) had anything to do with the origin of strabis- angle of the orbital axes.5 The eyes may also be mus, as has occasionally been claimed, is unlikely aligned in death.5 The position of the eyes in death since Hippocrates had used the word 400 years is determined by the absence of nervous impulses earlier. Perhaps Strabo had strabismus and thereby to extraocular muscles. Curare or curare-like sub- got his name. stances, which inhibit transmission at the neuro- muscular junction, can be used to artificially re- Relative and Absolute produce this situation in normal subjects. Toselli24 Position of Rest did this and found that the eyes assumed a position of 8Њ to 12Њ of divergence and 3Њ to 6Њ of elevation, The position assumed by the visual axes when which is comparable to the position assumed by fusion is suspended has been termed the relative the eyes in general anesthesia. Using a linear mea- Classification of Neuromuscular Anomalies of the Eyes 129 surement, Meyers17 determined the position of the tropia is present when the is negative eyes of 37 patients under general anesthesia who upon covering either eye in the absence of ambly- were undergoing some type of general surgery. opia. The latter qualification is necessary to ex- The state of ocular alignment had been previously clude patients with and eccentric fixa- tested. She found a significant degree of diver- tion in whom the cover test may also be negative gence in all patients who had been exophoric but in whom the visual axis of the amblyopic eye before being given anesthesia, as well as in one is not aligned with the object of regard (see Chap- third of patients with . The eyes of most ter 14). In Greek, orthos means ‘‘straight’’ or (65%) esophoric patients were parallel within the ‘‘correct’’ and, according to Lang,13 tropos means limits of accuracy of the method; a convergent ‘‘turn’’ but also ‘‘direction.’’ Thus orthotropia con- position was seen only in some patients with eso- veys the notion of a correct direction or position tropia. The position of the eyes in patients with of the eyes. Another acceptable term is orthoposi- strabismus who are under general anesthesia is tion,3 the position of the eyes in which the visual considered of importance by some surgeons in axes intersect at the fixation point under the influ- deciding how much surgery to do. This matter is ence of fusion. Both orthotropia and orthoposition considered further in the discussion of principles may be used interchangeably to describe binocular of surgery on extraocular muscles (see Chapter alignment on a fixation target. The term orthopho- 26). ria is not a good one since, as mentioned above, orthophoria is the exception and heterophoria is the rule in normal binocular vision.1 The terms Ocular Alignment straight-appearing eyes or straight eyes, which all too often seem to escape editorial scrutiny in the Ideally, the fusion-free position of the eyes should contemporary American literature, are to be be such that the visual lines are parallel in distance avoided. They lack precision in describing the fixation and have the proper convergence in near functional state of the patient since they encom- vision. This ideal, termed orthophoria, is infre- pass a whole spectrum of conditions that includes quently realized; it is only approached more or orthotropia, heterophoria of varying degrees and less closely. Whenever fusion is suspended by clinical significance, and even microtropia and some means, there is usually a deviation of the heterotropia with a small angle. visual axes even though it may be too small to be measured by ordinary clinical means. Orthophoria therefore is not a normal condition Direction of Deviation in the majority of people free from ocular symp- toms. Consequently, many clinicians consider a There are a variety of heterophoric or heterotropic certain amount of heterophoria to be normal. Mo- deviations (Fig. 8–2). If the visual axes converge, ses,18 for example, stated that 1⌬ to 2⌬ of esophoria the condition is called esophoria or esotropia, or 1⌬ to 4⌬ of in distance fixation should and if they diverge it is known as exophoria or be considered physiologic. He went on to say that . Hyperphoria or occurs if hyperphoria of 1⌬ of either eye nearly always one visual line is higher than the other. It is produces symptoms; hence, only 0.5⌬ of hyper- present on the right if the right visual line is phoria can be considered to be within the physio- higher than that on the left and on the left if the logic range. These values are selected on the basis left visual line is higher than that on the right. of clinical significance. A clinically significant One may also speak of a left hypophoria or finding is one that may produce symptoms and hypotropia when the right visual line is the higher may require treatment. It should be noted that the one and of a right hypophoria or hypotropia when clinical significance of heterophorias depends not the left visual line is the higher one. Since devia- so much on their absolute values as on correlated tions of the visual lines are relative, the terms findings, for example, the fusional amplitudes (see hypophoria and hypotropia may appear to be su- Chapter 4). perfluous, but they are useful, especially in hetero- For a description of a complete alignment of tropias, to indicate which eye is fixating. Thus the visual axes with the object of regard and thus right hypertropia indicates that the (lower) left of a desirable endstage of strabismus therapy, the eye is the one fixating, whereas left hypotropia term orthotropia appears most suitable. Ortho- indicates that the (higher) right eye is fixating. For 130 Introduction to Neuromuscular Anomalies of the Eyes

FIGURE 8–2. Classification by direction of deviation. A, Right esotropia. B, Left exotropia. C, Right hypertropia associated with small exotropia. D, Left hypertropia. E, Right hypotropia. F, Left hypo- tropia. G, Right incyclotropia. H, Right excyclotropia. the vertical heterophorias or heterotropias, then a convergent strabismus; an exotropia, a di- Bielschowsky2 also used the terms positive (right vergent strabismus; a hypertropia, a vertical stra- hyper-) or negative (left hyper-) vertical diver- bismus; and a , a torsional strabismus. gence (or deviation) in his American publications. The terms convergent and divergent strabismus, These terms are still in common usage in German which are widely used in the continental European . literature, have not become popular in this country. A misalignment of one or both eyes around the This is rather fortunate since convergent and di- sagittal axis produces clockwise or counterclock- vergent could easily be misunderstood to mean wise rotations of the (cyclotropia). Since the that the convergence or divergence mechanism is direction of the deviation must be defined in each implicated. Although this may well be so in some eye, the terms right or left excyclotropia or in- forms of horizontal strabismus, it certainly does cyclotropia are used. Cyclodeviations are mostly not hold true for others. In American usage the manifest; hence, differentiation between cyclopho- term strabismus generally is understood to be syn- ria and cyclotropia is difficult to justify on clinical onymous with heterotropia. In British and conti- grounds (see Chapter 18). nental European usage, the word includes both As already stated, deviations of the visual axes heterotropias and heterophorias. To differentiate also frequently are referred to by the time-honored between the two, the expressions manifest strabis- names of strabismus and squint. An esotropia is mus and latent strabismus are used. To encompass Classification of Neuromuscular Anomalies of the Eyes 131 both the heterophoric and heterotropic forms, such inadequate to keep the eyes properly aligned under terms as esodeviation and exodeviation are appro- any circumstances. One then speaks of a constant priate. deviation (constant strabismus, constant esotropia, A person may manifest a heterophoric or heter- constant exotropia). In other patients the fusion otropic deviation that combines two or more of mechanism functions well in some but not in all the various directions mentioned. He or she may circumstances. The deviation then is manifest only then have an esohyperdeviation,anexohyperdevia- at certain times, when the patient awakes from a tion,oracyclovertical deviation. nap or is tired, ill, under stress, or in particular test situations. An intermittent deviation (intermittent strabismus, intermittent esotropia, intermittent ex- Comitance and Incomitance otropia) is then said to be present. Even though variations may exist between different teaching Strabismus may occur in one of two major forms: hospitals, the symbols listed in Table 8–1 are fairly comitant incomitant it is either or . In comitant uniformly used for abbreviation of strabismus strabismus, the deviation is, within physiologic forms in charts and orthoptic records. limits and for a given fixation distance, the same Some patients display a heterophoric deviation in all directions of gaze. In incomitant strabismus, for one fixation distance and a heterotropic devia- one or more extraocular muscles show signs of tion for another fixation distance (e.g., esotropic underaction or paralysis. The deviation therefore in near vision but esophoric in distance vision). varies in different directions of gaze but is larger Patients with a paralyzed muscle may be hetero- when the eyes are turned in the direction of action tropic in one direction of gaze but heterophoric in of the underacting or paralytic muscle. Further the opposite direction. Also, patients with an A or differentiation between these two forms of strabis- V pattern of fixation (see Chapter 19) may be mus is discussed in Chapter 20. heterotropic in the position of maximum deviation The term comitant originally had the form con- and heterophoric in the position of minimum devi- comitant, derived from the late Latin concomitor, ation. In British usage,15, p. 94 following the lead meaning ‘‘I attend,’’ ‘‘I accompany,’’ which im- of Chavasse,4 this behavior is termed periodic plies that despite the deviation, one eye accompa- strabismus, meaning that during the period when nies the other in all its excursions (compare the the eyes are in a certain position a manifest stra- German Begleitschielen, concomitant squint). bismus occurs. The term is not well chosen, since Duane6 suggested comitant, a form which is uni- the word ‘‘periodic’’ generally refers to divisions versally accepted in the American literature and of time. In these cases the essence is not the time not without linguistic justification. during which a certain position of the eyes is We speak of incomitance when the angle of assumed, nor is there any periodicity. It is the deviation changes in different positions of gaze. position of the fixation object in space that deter- Incomitance may be caused by innervational fac- mines the sensorimotor response. tors (paralytic strabismus) or mechanical-restric- Cases of cyclic heterotropia (see Chapter 21) tive factors. represent an interesting variant of the intermittent type of deviation. In these patients a manifest Constancy of Deviation deviation appears at regular intervals (e.g., every other day). At the time when the eyes appear to A manifest deviation need not be present at all be straight, no latent deviation comparable in times. In some patients the fusion mechanism is amount to the manifest deviation can be measured.

TABLE 8–1. Common Abbreviations

Heterophoria Heterotropia Intermittent Near Distance Near Distance Near Distance

Esodeviation EЈ EETЈ ET E(T)Ј E(T) Exodeviation XЈ XXTЈ XT X(T)Ј X(T) Right hyperdeviation RHЈ RH RHTЈ RHT RH(T)Ј RH(T) Left hyperdeviation LHЈ LH LHTЈ LHT LH(T)Ј LH(T) 132 Introduction to Neuromuscular Anomalies of the Eyes

By classifying these patients with the general tropia as ‘‘bilateral strabismus.’’ The latter term group of intermittent strabismus, we do not imply should be reserved for those rare cases in which that the mechanism is the same as that in ordinary both eyes are deviated from the primary position intermittent esotropia or exotropia. (e.g., skew deviations, myogenic or mechanical strabismus). The term monofixation introduced by Parks20 to State of Systems describe what Lang12 referred to as microstrabis- mus or microtropia (see Chapter 16) is somewhat The role of accommodative convergence in de- ambiguous. It implies that only one eye is fixating. termining the relative position of the visual axes However, that is also the case in other forms of has been discussed in Chapter 5. Its role in the strabismus. Monofixation could also be interpreted etiology of esotropia and in the clinical picture of as lack of alternation. heterotropias is examined in later chapters (see Chapters 9 and 16). In this chapter mention will be made only that a further classification distin- Time of Onset of Deviation guishes accommodative esotropia from nonaccom- modative esotropia. In accommodative esotropia A deviation noted at birth or in the first months the act of has a major influence of life is termed congenital (connatal). Because on the deviation, whereas in nonaccommodative the onset is difficult to document at that age (see esotropia it does not. Chapter 16), the term congenital has been replaced Convergence is more active in near fixation by or is used synonymously with infantile, which and divergence in distance fixation. On this basis includes all forms of strabismus with an onset Duane6 developed his classification of the comi- during the first 6 months of life. If the deviation tant motor anomalies. If an esodeviation is greater arises after that age, it is called acquired. A variant at near than at distance, one may speak of a of the acquired form is acute esotropia (see Chap- convergence excess type; if an exodeviation is ter 16). These forms are also spoken of as primary greater at near than at distance fixation, then it is heterotropia. The meaning of the term secondary referred to as a convergence insufficiency type.If heterotropia is not quite uniform. In general it an exodeviation is greater at distance than at near, refers to a deviation that results from some known there is a divergence excess type; if an esodevia- cause such as a sight-impairing disease or trauma tion is greater at distance than at near, there is a of one eye (sensory heterotropia), or after surgical divergence insufficiency type.Wefind this classi- overcorrection (consecutive heterotropia). Occa- fication useful provided it is clearly understood sionally an esotropic eye may change spontane- that this terminology is to be used only in a ously into an exodeviation, in which case the term descriptive sense, that is, without etiologic impli- consecutive deviation is also used. cations. This classification is described in more detail in Chapter 17. Paralytic Strabismus

Type of Fixation Paralysis and Paresis The use made of the eyes for fixation is another If the action of a muscle or a group of muscles is important criterion for classifying heterotropias. completely abolished, this condition is a paralysis One distinguishes unilateral heterotropias (e.g., or palsy; if the action of the muscle or muscles is right esotropia or exotropia), in which the patient impaired but not abolished, this is a paresis.Itis habitually uses one eye for fixation, from alternat- not always possible to distinguish on clinical ing heterotropias, in which the patient fixates with grounds between paresis and paralysis since an either eye. A whole spectrum of fixation habits apparently paralysed muscle may occasionally re- exists, ranging from extreme unilaterality to free gain some function after surgery or Botox (botuli- random alternation. The term nonalternating stra- num toxin, type A) injection of its antagonist. bismus is preferable to ‘‘unilateral strabismus.’’ Inability to move an eye in a certain gaze direction Unilateral is the contrary of bilateral. It would does not automatically imply that the muscle in- seem inappropriate to define an alternating hetero- volved is paralyzed, as mechanical factors may Classification of Neuromuscular Anomalies of the Eyes 133 also impede ocular motility. In that case the term Orbital Strabismus paralysis, which should be limited to an innerva- tional cause of restricted motility, is inappropriate. Any ocular misalignment caused by anomalies of the or of the face (craniofacial dysostoses, plagiocephaly, hydrocephalus, heterotopia of mus- Muscles Affected cle pulleys, and so forth) may be referred to as orbital strabismus. The terms N III, N IV, and NVIparalysis refer to paralyses of muscles supplied by those cranial REFERENCES nerves. 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