Short Notes About Extraocular Muscles Anatomy

The extraocular muscles (EOMs) are composed of seven muscles: 4 recti, 2 obliques one levator palpebrae superioris (LPS) muscle. Figure 1 illustrates an anterior view of the EOMs and their relationships to one another. The lateral rectus receives innervation by CN VI (abducens); and the superior oblique receives innervation by CN IV (trochlear); and all the other muscles receive innervation by CN III (oculomotor). CN III has two divisions; superior and inferior: the superior division gives innervation to LPS and superior rectus muscles, while the inferior supplies the medial and inferior recti and inferior oblique. The sphincter pupillae and ciliary muscle receive their parasympathetic innervation via the lower division of CN III supplying the inferior oblique muscle [1].

Strabismus

Strabismus is a term describing any binocular malalignment. Esotropia (ET) and exotropia (ExT) are the most common types. ET is a convergence malalignment of the visual axes [3]. ET can be classified according to age of onset or its causes [4]:

• Infantile esotropia

• Acquired esotropia

• Accommodative esotropia

• Accommodative refractive esotropia

• Accommodative refractive esotropia with a high accommodative convergence to accommodation ratio AC/A

• Accommodative non refractive esotropia with a high AC/A ratio

• Partially accommodative esotropia

• Non accommodative esotropia

• Others

Infantile ET (IET)

IET presents before six months of age, however, intermittent ET during the first three months of life may be seen and does not necessarily indicate developing permanent ET. Children with IET are at risk for becoming amblyopic, however, cross-fixation may decrease the risk. Criteria of IET include the following [5]:

• Starts before the age of six months and does not resolve spontaneously

• The angle is usually fairly large and stable

• Fixation in most infant is alternating in the primary position

• Non-accommodative, sometimes partial accommodative 

• Deviation angle does not decrease and may increase with time

• Cross-fixation is frequent 

• Aberrant binocular functions

In addition, they may develop later latent or manifest latent nystagmus, inferior oblique overaction (IOO), A or V pattern strabismus, dissociated vertical deviation (DVD) and asymmetrical pursuit movement in optokinetic nystagmus between nasal compared to temporal [6].

Acquired ET

Typical of them to present following six months of age and may be full, partial, or nonaccommodative. Those patients exposed to significant risk for being amblyopic [7].

Accommodative ET (AET)

Criteria of AET include:

• Hypermetropia is usually associated with an accommodative, through exaggerated convergence in a child with bilateral hypermetropia (often >two diopters [D), which can be eliminated by correcting the refractive error (accommodative refractive ET) [8]

Figure 1: Frontal View of EOMs of the Left Eye [2]

• Typically, onset from 1-8 years, average around two years; it may appear in infancy or as a consequence of surgical correction of IE. Binocularity might be intact before the onset of strabismus [9]

• Often preceded by illness, elevated body temperature, or minor trauma [10]

Sometimes correction of the hypermetropia leads to orthotropia for far fixation but an ET at near (refractive AET with a high AC/A ratio). Occasionally, a child may have orthotropia for far with insignificant hypermetropia, however having a constant or intermittent ET at near (nonrefractive AET with a high AC/A ratio) [11].

Partially AET

Patients experiencing partial improvements of their ET if wearing glasses correcting their hypermetropia [4].

Non-accommodative ET

Patients with non-accommodative ET have acquired ET which nearly the same degree at far and near fixations without significant refractive errors or not improving after correcting the refractive errors. Neuroimaging is indicated with acute cases, specially if accompanied by double vision [12].

Other Types of ET

Other causes for ET in children include: CN VI palsies, unilateral type I Duane, sensory ET, restrictive ET, consecutive ET and nystagmus blockage syndrome [13].

Epidemiology

Esodeviations occur in equal frequency in males and females and they are more common in Caucasian and African American ethnic groups than in Asian ethnic groups in the United States. Factors that increase the risk for development of ET include anisometropia and hyperopia, neurodevelopmental impairment, prematurity, low birth weight, craniofacial or chromosomal anomalies, maternal smoking during pregnancy and family history of squint. With increasing age, the prevalence of ET increases (higher at 48-72 months in comparison to6-11months), different refraction between the two eyes and moderate degree of hypermetropia [14]. There are observations of a mendelian inheritance patterns. Amblyopia develops in approximately 50% of children who have ET. Esodeviations can result from innervational, anatomical, mechanical, refractive, or accommodative factors. There are several major types of esodeviations and they can be classified as comitant or incomitant [13].

Pseudo-ET

Pseudo-ET refers to the factitious appearance of ET when the visual axes are actually aligned, it caused by a flat, broadened nasal bridge; prominent epicanthal folds, negative angle kappa, or a low interpupillary distance. A person sees less sclera on the nasal side than usual, which makes the impression that the eye is turned inwards. This becomes more noticeable with lateral gazes. Since no real deviation exists, results of both corneal light reflex and cover tests are normal [1].

Risk Factors

Patients are at higher risks to develop squint if there is different refraction between the two eyes and/or hypermetropia, the higher the degree of hypermetropia the greater the risk to develop ET [15]. Other risk factors include children with neurodevelopmental impairment (like cerebral palsy); prematurity; low-birth weight [16]; low Apgar score; have craniofacial or chromosomal anomalies; children of smoker or alcoholic mothers and those with family history of squint [17,18].

Studying large number of mono and dizygotic twins revealed that inheritance for ET may be evidenced, but not for exotropia [19]. Another study investigated some risk factors in premature infants and reported that birth weights below 2Kg increased the risk of strabismus, while not related to gestational age independently [16]. On the long term, reducing or preventing these factors may lead to decrement the incidence of infantile ET [20].

Clinical Evaluation

Key questions for the clinician to ask when obtaining a strabismus history include the following [1]:

• At what age did the deviation or abnormal head posture (AHP) appear? (Reviewing old photographs may be helpful) Did onset coincide with trauma or illness

• Is the deviation or AHP constant or intermittent? Is it present for distance or near vision or both

• Is it present only when the patient is inattentive or fatigued? Is it associated with double vision or eyestrain

• If a deviation is noted, is it present in all positions of gaze? If a deviation is noted, is it unilateral or alternating

• Does the patient close 1 eye (squint)

• Is there a history of other ocular disease or ocular surgery

Diagnostic Positions of Gaze

They are a core set of 9 gaze positions used in the comprehensive assessment of ocular alignment. They consist of [21]:

• Primary position: The eyes fixate straight ahead on an object at infinity, which, for practical purposes, is considered to be 6 m, or 20 ft. For this position, the head should be straight. 6 cardinal positions: Two muscles (1 in each eye) are the prime movers of their respective eyes into each of these positions of gaze 

• Straight up and straight down: These do not isolate any single muscle, because the actions of both oblique and vertical rectus muscles affect elevation and depression from primary position

• Near fixation (usually 33 cm in the primary position) and reading position (depending on the patient’s symptoms) complete the list of clinically important test positions

Cover Tests

The tests should be done at far and near, with and without refractive correction [22]: 

• The monocular cover-uncover test: A pivotal examination to detect manifested squint and to distinguish a heterophoria from a tropia. As the target is viewed, one eye is covered and the opposite eye examined for any movement, which would indicate a heterotropia. Occluder is then removed. If there is no refixation of the non-covered eye when the occluder is introduced, moving of the covered eye in one direction with application of occluder, then in the opposite way (fusion refixation) with removal of occluder indicating a heterophoria. When patients have a heterophoria, their eyes would be aligned prior/following the examination; because squint appeared only during examination because the binocular vision was interrupted. While in heterotropia patients start with deviated eye(s) and, following examination, the original eye deviated in they have unilateral tropia or the opposite eye deviated if they have alternating heterotropia. In patients with intermittent heterotropia, the eyes may be straight before testing but become dissociated after occlusion

• The alternate cover test detects both latent (heterophoria) and manifest (heterotropia) deviations. As the patient views the target, the examiner moves the occluder from one eye to the other, observing the direction of movement of each eye when it is uncovered. Because this test disrupts binocular fusion, dissociating the eyes, this test cannot differentiate between latent and manifest parts

• Prism alternate cover test, prisms of varying amount are held over one eye or both eyes during alternating cover test; the amount of prism that neutralizes the deviation, such that eye movement is no longer seen as the occluder is moved from one eye to the other, represents the magnitude of the deviation. Horizontal and vertical prisms might be needed. Measurement of the total amount of deviation (heterotropia plus heterophoria)

• The simultaneous prism-cover test: Placement of a prism before the deviated eye and a cover in front of the fixated eye simultaneously. The procedure is done repeatedly using higher prism degrees until neutralizing movement. It has specific benefits for mono-fixation syndrome. Using binocularity viewing, those suffering from mono-fixation syndrome usually utilize peripheral fusion for controlling the squint partially. The heterotropia only is measured by this examination and it gives the accurate estimation for deviation amount in real-life.

Corneal Light Reflex and Red Reflex Tests

• The Hirschberg test: The Hirschberg test is principled on the relationship between the distance corneal light reflex from pupil center and the tropia. This ratio is about 22 prism diopters (Δ) per millimeter of decentration but can vary between 12Δ and 27Δ. In children who don’t cooperate it is difficult to measure the light reflex displacement in good accuracy, therefore estimations of the deviation are taken roughly, however these are largely dependent on the size of pupil: 30Δat the pupil margin, 60Δ in the middle of the iris and 90Δ at the limbus [23]

• The Krimsky test: Utilizing prisms for quantification of the deviation of the corneal reflection of a light source. Originally prisms were put before the deviated eye, however, modified recently by putting prism infront of the fixated eye and deviation is approximately measure by adjusting the prism power until the corneal reflections have symmetrical position

• The Brückner test: In the Brückner test by using the direct ophthalmoscope for obtaining a red reflex at the same time in both eyes. When the light reflex is shin on the fovea, the red reflex dims. If there is squint, fixating eye would have a dimmer light reflex compared to defoveating eye. Media opacities and refractive errors can also cause unequal red reflexes. Simultaneously, the positions of the corneal light reflexes can be assessed. This test should be used by primary health care physicians for screening for vision disorders

Subjective tests of Ocular Alignment

• The Maddox rod test assesses ocular alignment using the patient’s perception of the relative position of the images seen by each eye. For the eye viewing through the Maddox rod, a multiple parallel cylinder converts a point light to line image perpendicular to cylinders. Like alternate cover testing, the test is dissociating and precludes fusion; thus, heterophorias and heterotropias cannot be differentiated. The test cannot assess alignment in individuals with anomalous retinal correspondence (ARC) or suppression 

• The double Maddox rod: Used for measurement of cyclo-deviations. Two Maddox rods are put in spectacle frames so it can be rotated vertically so for the patient to see two horizontal lines. A small vertical prism may be introduced for separating the lines. The rod axes are rotated until parallel lines are seen by the patient. The angle of rotation indicates the orientation and amount (inside outside rotation) of cyclo-deviation. Usually, a red Maddox rod and a non-colored one are used, but this was thought to bias the patient’s localization of the cyclo-deviation toward the eye with the red rod. Using the same color bilaterally avoids this bias. In some cases, like congenital superior oblique palsy, patients mayn’t have subjective appreciation of cyclodeviation or indication of any torsion using this test. In such conditions, indirect ophthalmoscope is used to see fundus torsion and can aid in diagnosis

• The Lancaster red-green test (and variants like the Hess and Lees screen tests) is useful for assessing ocular alignment in complicated incomitant strabismus in cooperative patients with NRC and no suppression, such as adults with acquired strabismus. Reversible red-green goggles, red-slit and green-slit projectors and a grid projected or marked on a screen or wall are used in the test. With the red-filter before an eye, the operator shines a red slit toward grid; then patients put the green slit for appearing over the red one. Corresponding orientations of each streak is written down. Then repeat the procedure again for the all nine gaze positions, reverting the colors to record deviations with the other eye fixating

• The major amblyoscope can be used to assess ocular alignment both objectively and subjective. It may be particularly useful in adult strabismus, as it allows neutralization of torsional diplopia to assess fusional responses and can help characterize ARC. Separate, different targets are shown to each eye simultaneously and the amblyoscope is adjusted until the patient sees the images superimposed. If patients have NRC, it’s possible to read deviations in all directions straightforwardly from the device adjusted scale

Study Design, Setting and Duration

A retrospective cross-sectional study done at Ibsar Center in Al-Najaf city, from January 2012 to June 2019. The data were collected from medical records of 81 patients who underwent surgical correction for esotropia and included: patients’ age, patients’ gender, type of operation, presence of amblyopia, DVD, degree of esotropia , type of esotropia and the main surgical outcome regarding alignment in the last postoperative follow up.

Inclusion Criteria

• All cases were operated by the same surgeon

• Any age group and different genders

• First surgical correction for esotropia

• Patients completed six months or more postoperatively

Exclusion Criteria

• Sensory esotropia

• Patients with neurological disorder or development delay

• Incomitant esotropia

• Patients who were not followed up regularly or loss of data

Ethical Considerations

This study was approved by the scientific counsel of the College of Medicine in university of Kufa. Approval was obtained from Ibsar Center and patients’ identities were not disclosed during the study.

Examination of Patients

Preoperatively detailed history was taken by the same surgeon then full ocular assessment was done which included visual acuity and refraction (Cycloplegic refraction by cyclopentolate 1% eye drops, one drop, repeated after 5 minutes and examined after 30 minutes [12] and Atropine eye drops (1%), for children younger than 5 years of age, has to be applied twice a day, 3 days before refraction) along with slit lamp biomicroscopy with +90 diopters condensing lens for posterior segment with detailed fundal examination, or by indirect +30 diopters condensing lens, then examined after the cycloplegia waned off for best corrected visual acuity, corneal reflex tests ,cover-uncover test ,alternate cover test ,prism cover test ,motility test and postoperative diplopia tests (PODT) for older and oriented patients.

Table 1: Amount of Recession and Resection That Was Used by Surgeon

After period of correction the refractive error and management of amblyopia surgery done for patients. The Table 1 was used by the surgeon for measurement of amount of recession and resection.

Follow Up

Eighty-one patients enrolled in this study and all of them had been followed up by the same surgeon after first postoperative day, one week, one months and six months. Examinations included visual acuity and refraction, motility test, cover-uncover test, alternating prism cover test, dilated fundal examination.

Definition of Variables

• Orthotropia: Esotropia equal or less than 10 prism diopters [24]

• Undercorrection: Esotropia of more than 10 prims diopters [24]

• Overcorrection: Exotropia of any degree [25]

Statistical Analysis

Data tabulation, input and coding was done by the use of IBM© SPSS© (Statistical Package for the Social Sciences) Statistics Version 23. Chi-square test was used to investigate the association between categorical variables. Normal distribution of numerical variables was tested by Anderson–Darling test and age in years and degree of esotropia pre-operatively did not follow the normal distribution, so Kruskal Wallis Test was used to test the difference between outcomes. p-value of 0.05 or less was considered significant throughout data analysis.

This study enrolled 81 patients with esotropia, their median age was five years ranging from 1 year to 37 years, 53.09% were males and 46.91% were females. Table 2, Basic criteria of the study population (Figure 2).

There were 63 (77.78%) patients with orthotropic outcome and 15 (18.52%) had under correction, while only 3 (3.7%) had overcorrection, as shown in Figure 3.

There was no statistically significant association between type of surgery and outcomes, as 86.7% of patients who had undercorrection had BMRR as shown in Table 3.

There was no statistically significant association between amblyopia and outcomes, although it can be noticed that 7 (46.7%) of amblyopic eyes patients had under correction (Table 4).

There was no statistically significant association between DVD and outcomes, as most patients with DVD were orthotropic (Table 5).

There was no statistically significant association between type of esotropia and outcomes and most patients with partially accommodative esotropia were orthotropic (Table 6).

There was no statistically significant difference between age and outcomes, as the median age in patients with orthotropia was 5 years (ranging from 1.4 to 36 years), compared to the 6 years in undercorrection and 3.6 years in overcorrection. There was no statistically significant difference in degree of esotropia preoperatively and outcomes, as the median degree was 40 prism diopter in patients who achieved orthotropia compared to 35 prism diopter in patients with undercorrection and 30 prism diopter in patients with overcorrection (Table 7).

Figure 2: Histogram Illustrating the Age-Distribution

Figure 3: Distribution of Study Sample According to Outcomes

Table 2: Basic Criteria of the Study Population

Table 3: Distribution of Type of Surgery According to Outcomes

*: Chi-square test with Fisher Exact test, MR: bilateral medial rectus recession, R/R: recession/ resection

Table 4: Distribution of Amblyopia According to Outcomes

Chi-square test with Fisher Exact test

Table 5: Distribution of DVD According to Outcomes

Chi-square test with Fisher Exact test, DVD: dissociated vertical deviation

Table 6: Distribution of Type of Esotropia According to Outcomes

Chi-square test with Fisher Exact test

Table 7: Differences Between Outcomes According to Age and Degree of Esotropia

Kruskal Wallis Test (Exact significance)

In the current study, there were 63 (77.78%) patients with orthotropic outcome and 15 (18.52%) had under correction, while only 3 (3.7%) had overcorrection. This was comparable to results of Idris et al. in Ireland who studied 75 patients with horizontal strabismus and followed them post-operatively and reported that 69.3% had less than 10 prism diopters (PDs) from orthotropia, 24% had 11-25 PDs and 4% had 25-35 PDs and 2.7% had very large post-operative degrees of more than 35 PDs [26]. In another study, done by Leffler et al. [27], in the United States of America (USA), who investigated 6,178 operations for different types of strabismus and reported that the reoperation rate was 6.5% [26]. Consecutive ExT is estimated in different studies to occur in 3-29% of cases [27,28], which could happen years after the first recession surgery and in about one third of cases the cause is slipped medial rectus muscle [27]. Another explanation for low overcorrection in the current study, was the fact that most surgeons are usually cautious not to cause overcorrection and shifting the patients to ExT, since micro-esotropia is desirable outcome [29,30], so undercorrection would naturally be more prevalent than overcorrection.

In the current study, 64(79%) had BMRR and 17 (21%) had R/R, with no statistically significant association to outcome, Idris et al. [26], in Ireland who reported that BMRR had a surgical effect on near deviation of (3.59 PD) for each mm recession and monocular R/R had a 3.66 PD/mm change in ocular deviation [26]. Similarly, Leffler et al. in the USA, reported no statistically significant difference regarding esotropia reoperation rate between operating two muscles in one eye (5.9%) compared to one muscle in two eyes (6.1%) [27]. BMRR is usually the preferred and most commonly done operation for esotropia [31], with different reports of success rates [32,33].

In the current study, amblyopia was seen in 31(38.3%) patients and 46.7% of patients who had under correction were amblyopic and DVD developed in 19.8% of patients, in which none had overcorrection and only 2 (13.3%) had under correction. This was comparable to results of, Idris et al. in Ireland, who reported that amblyopia affected 45.3% [26]. In another study done by Wan et al. in USA who studied 88 patients with large angle infantile esotropia and reported an overall success rate of only 23% (defined by less than 10 PD esotropia) and reported that amblyopia was not associated with increased risk of failure, also they reported that DVD developed in 24% of patients [24]. In addition to another study done by Magli et al. in Italy, who studied 525 with infantile esotropia and reported that 26.86% had amblyopia and 28.76% had DVD and both were not associated with reoperation rate (34). This can be explained as DVD is considered a marker for disruption of binocularity and since the primary goal of strabismus surgery is to restore binocular single vision in children, so the presence of DVD preoperatively or its development postoperatively might influence the final outcome, related to this concept Arslan et al. in Turkey reported that early surgery for infantile esotropia was associated with a lower rates for developing DVD [35], Shin an Paik in Korea reported that surgery for infantile esotropia before two years of age decrease the incidence of spontaneous DVD [36]. While Yagasaki et al. in Japan reported that early surgery for infantile esotropia decreased the severity of DVD rather than the incidence of DVD [37].

In the current study, there was no statistically significant association between type of squint and postoperative outcome and in our study, neither age nor degree of esotropia preoperatively were related to outcomes. Kim and Choi in South Korea investigated factors affecting outcomes of patients with acquired nonaccommodative esotropia in 35 patients and reported that the mean angle of deviation postoperatively was 4.2 PD at day 1, 3.9 PD at month 3, 4.7 PD at year 1 and 4.8 PD at final follow-up, indicating a small increment in deviation over time and also they reported that none of the preoperative variables had a statistically significant effect on outcome, which included; gender, age at onset, preoperative degree of esotropia, age when of having the surgery, spherical equivalent, amblyopia, fusion by Worth-4-dot, preoperative follow-up period, or type of surgery [84]. While for congenital esotropia, Louwagie et al. in USA studied 130 children diagnosed with congenital esotropia and reported that 38.6% of them had amblyopia, 2.3% had DVD and 45% had successful (within 8 PD) correction and they found that second surgery risk factors included larger presenting angle and younger age at first surgery [38,39].

Limitations of the Current Study

This study enrolled all age groups, who would have different etiologies and management goals/plans. Due to the retrospective nature of the study, limited variables were obtained, so other targets for operations like; amblyopia improvement, diplopia (preoperative/postoperative) and cosmetic outcomes were not assessed.

• The outcomes regarding ocular alignment in the current study were satisfying and comparable to other studies in the world

• Age, gender, degree of esodeviation preoperatively, type of surgery, type of squint, amblyopia or DVD were not associated with surgical outcome regarding alignment

Recommendations

• Further studies should be done regarding other outcomes for esotropia, including improving stereopsis, cosmetic, or relieving of diplopia

• Larger sample is needed with longitudinal follow up to investigate factors related to surgical outcomes

• It is important to tell the patient that there is no guarantee to be orthotropic after first surgery and multiple surgery may be required

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