A 1-Year Review of Amblyopia and Strabismus Research.

ANNUAL REVIEW

A 1-Year Review of Amblyopia and Strabismus Research Michela Fresina, MD and Emilio C. Campos, MD

Purpose: This current review highlights some of the literature published in the past year from April 2013 to May 2014.

Design: Literature Review. Methods: The present review is based on an extended search for pertinent articles on amblyopia and strabismus published during the specified period. Results: Many articles are often not very comparable to one another because of a lack of randomized clinical trials with most of the studies being retrospective in nature. There is often disagreement on some terminology. Typically, the definition of binocular vision is rarely related to the tests used for evaluating it. Conclusions: The authors conclude that adult strabismus patients seem to gain benefits from corrective surgery not only for their ocular misalignment, but also for social anxiety levels that may be associated with improvements in their quality of life and disability levels. Key Words: amblyopia, strabismus, Duane syndrome, Brown syndrome (Asia-Pac J Ophthalmol 2014;3: 379Y387)

PART I: AMBLYOPIA Neurological and Neuroanatomical Changes in Amblyopia In a recent study, the group of Niechwiej-Szwedo et al1 tried to characterize the effects of amblyopia etiology and the severity of the acuity and stereoacuity deficits on eye movements and visually guided reaching movements. They found that strabismic amblyopes had longer reach latency during amblyopic eye viewing when compared with anisometropic amblyopes with reach latency comparable to visually normal subjects across all viewing conditions. The results might be due to a greater central suppression of the deviated (amblyopic) eye in strabismic amblyopia. They also found that reach precision and accuracy are reduced only in amblyopes without stereopsis, regardless of whether the visual acuity (VA) loss is mild or severe, supporting the idea that patients with negative stereopsis have larger deficits in localization precision. Raashid et al2 measured the spatial and temporal characteristics of saccadic adaptation in response to visual errors. The generation of adequate saccades, despite diseases and physiological changes, depends on a continuous recalibration of the oculomotor system by visuomotor adaptation mechanisms. These mechanisms process errors in motor performance and update From the Department of Ophthalmology, University of Bologna, Bologna, Italy. Received for publication July 17, 2014; accepted October 19, 2014. The authors have no funding or conflicts of interest to disclose. Reprints: Emilio C. Campos, MD, Ordinario di Malattie dell’Apparato Visivo Direttore della Scuola di Specializzazione in Oftalmologia Alma Mater Studiorum, Universita` di Bologna Direttore dell’U.O. di Oftalmologia Policlinico S.Orsola-Malpighi via Palagi, 9, 40138 Bologna, Italy. E-mail: [email protected]. Copyright * 2014 by Asia Pacific Academy of Ophthalmology ISSN: 2162-0989 DOI: 10.1097/APO.0000000000000097

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the relationship between a visual target location and the motor commands that are necessary to look at this target. In their work, a saccadic adaptation was induced using a paradigm that simulates a spatial error in saccadic generation by systematically shifting the visual target during saccade execution. The rapid (short-term) saccadic adaptation elicited by the target paradigm has been previously recognized as a valuable model of the long-term adaptation described in pathological conditions. The authors observed that short-term adaptation of a saccadic gain (the ratio between the saccade amplitude, which is the distance traveled by the eyes; and the desired saccade amlitude, which is the distance of the target from the initial eye position) was weaker and more variable. Saccadic latencies were longer, and saccadic gains and latencies were more variable in patients with anisometropic amblyopia during amblyopic eye and binocular viewing. They propose that this impaired adaptation results from a reduced capability of the saccadic motor commands to be modified accurately because of imprecise postsaccadic error signals as a result of amblyopia-related visual losses. This supports the proposal that the error signal driving saccadic adaptation is visual. Kanonidou et al3 investigated eye movements in strabismic amblyopia and found that strabismic amblyopes make more saccades per line than controls without significant changes in saccadic amplitudes, irrespective of the font size and the viewing conditions. These findings suggest that ocular motor deficits that exist in strabismic amblyopia during reading, when VA is not a limiting factor, are not related to crowding. Magnetic resonance imaging (MRI) continues to be studied in amblyopia. Ding et al4 investigated the characteristics of the functional connectivity pattern of the primary visual cortex and other brain areas in a relatively small sample size of patients with anisometropic and mixed (anisometropic and strabismic) amblyopia by means of functional MRI (fMRI). The authors mainly found significant decreases in functional connectivity with the primary visual area in the inferior parietal lobule and the posterior cerebellum in both anisometropic amblyopia and mixed amblyopia. This finding provides further evidence for the disruption of the dorsal visual pathway in amblyopic subjects. Anatomical changes in gray and white matter in monocular amblyopia were investigated by Li et al,5 analyzing MRI brain images using a particular imaging technique. Volume loss in cortices related to spatial vision and growth in the gray and white matter volume in the occipital lobe and precuneus were found in monocular amblyopes compared with matched controls. The involvement of cortical areas in the volume loss would provide neuroanatomical evidence of stereoscopic defects, whereas the growth may reflect a compensation effect by the unaffected eye.

Detection and Referral: Conditions Associated With Amblyopia In a cross-sectional survey reported in October 2013, the prevalence of amblyopia was the same (1.81%) in Asian and non-Hispanic white children aged 6 to 72 months. It seemed to be higher among older non-Hispanic white children but relatively stable by age in Asian children.6 Pascual et al7 in the Vision in Preschoolers Study found that strabismus and refractive

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errors were risk factors for unilateral amblyopia whereas bilateral astigmatism and bilateral hyperopia were risk factors for bilateral amblyopia. These results, despite differences in the selection of the study group, validated the findings from the MultiEthnic Pediatric Eye Disease Study. In the Sydney Pediatric Eye Disease Study, the authors found an increasing risk of anisometropia with higher myopia (Q j1.0 diopters [D]), hyperopia (Q + 2 D), and astigmatism (Q1.5 D). In their preschool age, population-based sample anisometropia was uncommon, with interethnic differences in cylindrical anisometropia prevalence. They also quantified the rising risk of anisometropic amblyopia with increasing spheroequivalent (SE Q 1.0 D) and cylindrical anisometropia and presented the specific levels of refractive error and associated increasing risk of anisometropia.8 In a metaanalysis of the major community preschool eye examination studies, Arnold9 estimates a set of risk factors for amblyopia. He states that the approximate prevalence of anisometropia is 1.2%, hyperopia is 6%, astigmatism is 15%, myopia is 0.6%, strabismus is 2.5%, and VA less than 20/40 is 6%. The mean combined prevalence is 21% T 2% compared with a prevalence of amblyopia with VA of 20/40 or worse of 2.5%.9 Griepentrog et al,10 in a population-based cohort study, reported the prevalence and causes of amblyopia among 107 patients with childhood ptosis diagnosed over a 40-year period. They concluded that occlusion of the visual axis was the leading cause of amblyopia in patients with congenital simple unilateral ptosis in this report. This finding is in contrast to large referral-based retrospective studies of congenital ptosis in which the leading causes of amblyopia were strabismus or significant refractive error.11Y14 The use of visual-evoked potential (VEP) in amblyopia has been previously reported, and the relationship between VEP and VA in amblyopes has been the subject of many articles. Halfeld Furtado de Mendonça et al,15 recently compared the patternreversal VEP responses of amblyopic eyes with those of sound eyes in 65 amblyopic children aged 2 to 13 years. Unlike what was found in other studies,16 the authors observed no statistical significant differences concerning P100 amplitude and latency for any stimuli between the amblyopic and the sound eye of amblyopic children. These findings may be consistent with the suggestion that the sound eye in amblyopic patients is not really functionally normal. Because we do not know yet with certainty the possible alterations in the healthy eye of amblyopic subjects and in reference to the variability of the effect of unilateral eye patching on VA of infants and children reported in a study in 1981 by one of the authors,17 Halfeld Furtado de Mendonça et al concluded that special attention should be paid to amblyopic treatment as patching can have a negative effect on the sound eye.15

Diagnosis The earlier detection and treatment of amblyopia can lead to a better vision prognosis, so it becomes particularly important to have amblyopia screening. The fundamental role of vision screening programs is emphasized by de Koning et al18 in a study that shows a reduced risk of persistent amblyopia at the age of 7 by more than 50% in children undergoing intensive eye examination. Arnold and Armitage19 evaluated the benefits of photo screening, especially in preverbal children, and concluded that even in high-risk and young children, current instrumentbased screeners can reliably screen for refractive and strabismic risk factors that lead to amblyopia. In 2011, Candy et al20 showed that in adult patients, relationships between VA obtained with different vision tests are similar to those that are reported in studies of children’s vision. Thus, to investigate the potential sensitivity of a range of charts in detecting amblyopia,

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Formankiewicz and Waugh21 measured the effects of increasing blur and retinal eccentricity on VA in adults with commercially available children’s vision charts and chart designs that incorporate features at different distances away from the target, including those closer than what is currently available commercially. Their results suggest that optimally designed crowded tests would be particularly helpful in the detection of amblyopia associated with strabismus or in patients who use eccentric viewing loci but less valuable in the detection of purely anisometropic amblyopia or in uncorrected refractive error. The crowding effect would be greater if flanking features are placed closer to the target than they currently are in commercially available charts. Fu et al22 evaluated the validity of uncorrected distant and near VA and stereoacuity for screening amblyopia in 2893 students in primary schools in central China, and their results showed that simultaneous testing of distant VA of low cutoff and stereoacuity was a sensitive and specific method. Huang et al23,24 introduced a new specialized VA chart consisting of 4 symmetrical shapes (triangle, square, cross, and circle) for amblyopic children aged 3 to 5 years. It should overcome an inability to recognize the letters in the alphabet and difficulties in designating the direction of black abstract symbols (Albini ‘‘E’’ or Landolt ‘‘C’’). The results of this study support the validity and reliability of distance VA measurements using the new eye chart that seems to be great for early detection of amblyopia. Finally, Chou et al25 confirmed that oblique astigmatism is more amblyopigenic than orthogonal astigmatism but equal resolution rates after longer refractive treatment were described in children with oblique astigmatismrelated refractive amblyopia.

Treatment Once all the possible organic causes (such as ptosis, cataract, etc) were removed and the best optical correction was prescribed, the classical treatment of amblyopia is based on the interruption of the visual input in the fixing eye to stimulate vision development in the amblyopic eye. However, sometimes this therapeutic approach proves insufficient, owing either to problems of compliance with patching treatment or to a tendency to lose over time the benefits obtained. Recent hot topics in the literature on amblyopia concern some important issues such as the correct patching regimens in relation to compliance with treatment, alternative methods of treatment, binocular therapy, and treatment options outside the plastic period. In a recent study, Repka and Holmes26 summarize some of the most important results obtained from Pediatric Eye Disease Investigator Group (PEDIG) through studies conducted years ago or still in progress. Spectacles alone are effective both in managing amblyopia, including strabismic amblyopia surprisingly, and in improving compliance with additional treatment, such as occlusion or penalization.27 No demonstrable advantage was found between lower and higher doses of patching, calculated for different degrees of amblyopia, both in magnitude and rate of improvement.28,29 Atropine treatment, in all tested doses, is as effective as patching in the active treatment of amblyopia. The only apparent limit is that subjects treated with atropine improve more slowly, until they become equated, however, to those treated with occlusion after 6 months of therapy.30,31 None of the known risks (amblyopia by deprivation) or adverse effects (from photophobia to poisoning) and none of the nonoccurrence of a change in fixation were described or emphasized. Moreover, a more precise statistical evaluation suggests that patching remains the most effective treatment for amblyopia. Finally, blurring Bangerter filters seem to be effective like occlusion and penalization as initial active treatment for * 2014 Asia Pacific Academy of Ophthalmology



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moderate amblyopia.32 Some comments on the study by Repka and Holmes were made by Lempert33 concerning the possibility that the inconsistent differences between the outcomes obtained from optical correction, low-dose patching, atropine, and Bangerter filters may invite exploration of the effect of no treatment. It must be emphasized that the results described concern only the anisometropic and strabismic amblyopia and cannot be extended to deprivation amblyopia. In North America, there is a general move from full-time to part-time patching after the PEDIG results were published. Jin et al34 investigated whether the evidence-based recommendations by the PEDIG, as initial treatment of amblyopia, have been implemented in clinical practice. The authors found that for the initial treatment of moderate amblyopia, the cohort was prescribed a mean hours of daily patching significantly greater than the recommended 2 hours, and only 24% of them were prescribed the recommended initial patching hours. For the initial treatment of severe amblyopia, the cohort was prescribed a mean hours of daily patching significantly lower than the recommended 6 hours, and only 12% of them were prescribed the recommended initial patching hours. Despite that, the results obtained in terms of VA seemed to reach the same values with a few months of difference. A prospective study by Sachdeva et al,35 comparing continuous wear to split hours part-time patching in anisometropic amblyopia, concludes that both patching regimens lead to significant and comparable improvement in best corrected VA (BCVA) up to 6 months of follow-up. The knowledge of the exact number of hours of occlusion used in the child, a prerequisite for determining a dose-response relationship, is still the basic factor for defining a therapeutic prescription regimen based on evidence.36Y40 Data from a previous study on the compliance with occlusion therapy in amblyopic children by means of a dose monitor41 showed that the mean compliance across all participants with the duration of follow-up was substantially lower than the prescribed dose. The longer the patient is in treatment, the lower the compliance. Moreover, compliance is not affected by age, sex, type, and severity of amblyopia, whereas it seems to be improvable by frequent controls. The last statement may seem at odds with what was stated by other authors who did not have satisfactory visual outcomes in amblyopic children despite many hospital visits and who found compliance a major problem.42 To minimize problems of compliance with occlusion therapy, various alternatives are proposed, such as liquid crystal glasses,43 the Amblyz eyeglasses, acupuncture,44 rotated prisms combined with near activity,45 and a computer-based interactive binocular treatment system (IBiT),46,47 which requires further experimentation on large numbers, perhaps through randomized controlled trials. Finally, data from a study by Ding and Levi48 demonstrate that reducing the dominant eye’s mean luminance reduces its suppression on the nondominant eye and therefore rebalances the asymmetric binocular vision. As a result wearing a neutral density filter before the dominant eye (or increasing the mean luminance in the nondominant eye) may be more beneficial than the traditional method of patching the dominant eye for treating amblyopia.48 Li et al49 evaluated the relationship between interocular suppression and visual function in anisometropic amblyopes and the relationship between interocular suppression and outcomes of occlusion therapy. They also studied if suppression can be simulated and the effects of different means of refractive errors correction estimated and reproduced. They state that interocular suppression plays a key role in the visual deficits associated with anisometropic amblyopia and can be simulated in controls by inducing a luminance difference between the eyes. Accurate quantification of suppression using the dichoptic motion coherence threshold technique may provide useful information for the management * 2014 Asia Pacific Academy of Ophthalmology

and treatment of anisometropic amblyopia.49,50 Great interest is found in the literature on stereopsis in amblyopia, although unfortunately there is often no correlation between the degree of stereopsis and the methods used to test it. Some authors studied the effects of amblyopia treatment on stereoacuity in anisometropic, strabismic, and mixed amblyopes and concluded that stereoacuity improved in all the 85 pediatric patients after an ‘‘optical treatment’’ possibly combined with occlusion. They also indicated poor VA of the amblyopic eye and large-angle strabismus as negative predictive factors.51 With regards to the determinants of response to amblyopia therapy, the grade of amblyopia and accommodation were confirmed to be fundamental,52 and older age, better BCVA after stopping therapy, and greater magnitude of improvement in BCVA were indicated to be important risk factors for recurrence of anisometropic amblyopia.53 A study by Althomali54 reports the outcomes of toric posterior chamber phakic intraocular lens implantation in 6 children aged 5 to 15 years for anisometropic amblyopia refractory to medical treatment, including spectacles and contact lenses. It is argued that the implantation of intraocular lenses in the anatomically healthy eye of patients with a long life expectancy could never be justified from an ethical point of view. New drug therapies for amblyopia treatment in children and adults were investigated in a study by Pescosolido et al.55 An interesting review by Antonio-Santos et al56 from Cochrane Database did not find any randomized or quasirandomized controlled trial evaluating the effect of occlusion or other treatments (pleoptic and Cambridge amblyopic vision stimulator [CAM] visual stimulation) for unilateral stimulus deprivation amblyopia. The authors conclude that there is a great gap in knowledge in this regard so that no evidence-based demonstration on the effectiveness of any treatment is available. As classical treatment focuses on improving the vision, with uncertain results in improving binocular vision, and some authors propose that a binocular disorder is primary with amblyopia as its consequence, new approaches have been proposed to recover VA in amblyopic adults. Two recent reports in the literature regarding perceptual learning substantially confirm the results from previous studies and state that perceptual learning is effective in improving amblyopic vision,57 mainly through rule-based cognitive compensation58 and stereovision57 assessed with the Fly Stereo Acuity Test in adult amblyopes. Ooi and He,59 in a previous study on binocular rivalry, suggested the role of voluntary attention in retaining the dominant image in visual awareness and that cuemediated involuntary attention could make a rivalry stimulus reaching visual awareness. They used their results to create a protocol of ‘‘push-pull’’ perceptual learning to reduce sensory eye dominance. It consists of an attention cue presented to the weak eye, preceding the binocular competitive stimulation, which stimulates the weak nondominant eye (push) while causing interocular inhibition of the strong dominant eye (pull).60 The stronger learning effect with the push-pull training compared with the push-only training (such as stimulating the weak eye while patching the dominant eye) underscored the crucial involvement of a putative inhibitory mechanism in sensory plasticity. Therefore, the authors applied the push-pull treatment for amblyopia in adults.61 Zhou et al62 propose a sort of ‘‘inverse’’ occlusion for 2.5 hours by a translucent patch in adult amblyopes. Their findings rely on reduced sensory stimulation and suggest a new type of plasticity that is both rapid and binocular. The benefits for binocular function reported are very robust although unaccompanied by consistent changes in monocular contrast sensitivity. According to the www.apjo.org


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authors, this is because monocular effects, unlike binocular effects, take more time to develop. Their approach returns validity to inverse patching as a promoter of an improvement in binocular function, considering the primum movens for the development of amblyopia. The results are interesting as regards a probable plasticity in adults with amblyopia, although the study involves only 8 adult amblyopes whose binocular sensory balance was measured within a maximum of 60 minutes after the removal of the patch. There are no data regarding the durability of the improvements achieved. The same authors in a previous study63 developed a novel way of quantifying suppression and found that when the signal presented to the fellow fixing eye was reduced in strength, strabismic amblyopes could combine information between their 2 eyes, as normal individuals do. Therefore, providing artificial viewing conditions under which binocular vision can take place leads to a strengthening of binocular vision itself, facilitating its operation under a wider variety of interocular viewing conditions. This finding provides the basis for a new binocularly based treatment of amblyopia in which the suppressive imbalance is measured and treated as a first step.64 In a more recent study,65 the same authors provide evidence that alleviating suppression of the amblyopic eye by means of prolonged periods of viewing of stimuli of different contrast in each eye (dichoptic stimulus), during which information from the 2 eyes is combined, induces greater levels of plasticity than a forced use of the amblyopic eye alone and leads to an eventual combination of binocular information under natural viewing conditions (stimuli of the same contrast in each eye). This would indicate that suppression is a key mechanism that prevents the amblyopic brain from learning to see. These findings could provide a basis for the treatment of amblyopia in adults who currently have no treatment options. On this basis, the authors demonstrated that a simultaneous transcranial direct current stimulation of primary motor or visual cortex, known to reduce inhibition of inputs from the amblyopic eye,66 enhances the therapeutic effect of dichoptic stimulation alone, leading to greater improvements in stereoacuity.67 There are some studies that support the therapeutic effects of darkness, eventually associated with repetitive visual stimulation,68 in an animal model of deprivation amblyopia.69 Because the benefits of darkness seem to be linked to its ability to reset the cortex to an earlier stage of development, impediments to clear concordant binocular visual input should be eliminated or substantially reduced before darkness is imposed. Otherwise, amblyopia may become worse. Potentially, darkness therapy may serve best to boost and hasten the outcomes of newly developed binocular therapies for amblyopia that could be implemented immediately after a period of darkness.

OCT Analysis It is known that the repeatability of the measurements obtained in the optical coherence tomography [OCT] is not good when studying children or teens. This is even more true when the retinal nerve fiber layer (RNFL) is studied. For this reason, the data obtained from the various measurements are not always comparable. Furthermore, the comparison groups are not always homogeneous with regards to the type of amblyopia, age, and antiamblyopic treatment of the patients examined. A thicker macula was found in macular OCT in anisometropic amblyopic eyes.70,71 Retinal involvement was not observed in the peripapillary nerve fiber layer of amblyopic eyes.71 With regards to RNFL OCT, the optic disk does not seem to be the site of morphological changes in anisometropic amblyopia72 in adults or in esotropic amblyopia in children.73 No

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significant differences in morphological and functional measures between amblyopic eyes in different types of amblyopia were found. However, in the combined and anisometropic amblyopes, ganglion cell complex was found to have increased compared with the control group.74 In the anisometropic group, the inter-eye differences in RNFL thickness parameters seemed to be related to the refraction differences between the amblyopic eyes and their fellow eyes.75 Macular and RNFL thicknesses seem to be more extensively associated with differences in the axial length and refraction than with amblyopic development, based on the fact that these thicknesses remained unchanged after amblyopic treatment.76

PART II: STRABISMUS Prevalence McKean-Cowdin et al6 estimated the prevalence of strabismus to be similar in Asian (3.55%) and non-Hispanic (3.24%) white children and higher among older children, from 6 to 72 months, in both racial groups.77

Pathophysiology As regards pathophysiology, a study by Joshi and Das78 investigated the role of cerebellar nuclei in conjugate eye movements and binocular eye alignment. It was already known that they were involved in vergence movements and accommodation control in normal monkeys, and the authors found that they are also involved in maintaining the steady-state misalignment in monkeys with strabismus.78 Yang et al79 tried to explore the neural basis of infantile esotropia and locate the cortical region of fusion function defects using blood oxygen level-dependent fMRI to measure the visual cortex response to a presented visual stimulus. They concluded that the activation of some cortical areas in fMRI could be compensatory for the fusion dysfunction.79 The limitations of this study may be that the conclusion is based only on the fact that nonstrabismic subjects did not show activation of these areas and that only 5 patients were examined.

Esotropia Silbert et al,80 in a retrospective analysis of 253 patients with follow-up, described a significant risk of esotropia development in children younger than the age of 3 years that were diagnosed with pseudoesotropia. No differences in risk were found in these pseudoesotropia patients with greater or less than 1.50 D of hyperopia. Their findings seem to be different from a previous study by Mohan and Sharma,81 who found a statistically significant difference in the development of accommodative esotropia between children with pseudoesotropia and greater than 1.50 D of hypermetropia (53.9%) and those with pseudoestropia and less than or equal to 1.50 D of hypermetropia (2.6%). Garretty82 evaluated the incidence of a manifest strabismus found at 5-year vision screening in children who were referred with concerns of strabismus under the age of 30 months and were initially diagnosed with either pseudostrabismus or ‘‘no abnormality detected.’’ She reports that the incidence of undiagnosed esotropia in her group was between 2.4% and 3.4%; therefore, the risk of failed vision screening was the same as that in the general population.82 With regards to interventions for infantile esotropia, an interesting review from the Cochrane Database highlighted the weaknesses of most of the literature on strabismus.83 The authors state that no studies were found to meet their selection * 2014 Asia Pacific Academy of Ophthalmology



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criteria because no randomized trials are present in the literature. They conclude that there is no agreement on the type of surgery (monolateral vs bilateral, standard recessions, or 3muscle surgery) for strabismus. There is no agreement on the role of age at intervention on preservation of binocularity with some suggesting ‘‘ultra early surgery’’ within 6 months, and some suggesting ‘‘later’’ surgery. No agreement is found on the successful use of early botulinum toxin injections on restoring the binocular state as compared with surgery and, as mentioned previously, there is a lack of homogeneity in the definition of binocularity. Park and Oh84 demonstrated stable eye alignment and binocular function after a maximal tolerable amount of spectacle undercorrection, up to j1.5 D, in patients with accommodative esotropia, in the 2-year follow-up. If these data are confirmed, full spectacle correction will no longer be considered as the most effective means of controlling the deviation and allowing for continued development of binocular single vision. It seemed to us that these data can be very reassuring for refractive surgeons operating on patients with accommodative esotropia who may undergo an undercorrection or a regression of the hyperopic treatment. With regards to consecutive esotropia, Park et al85 demonstrated good results after unilateral lateral rectus advancement with medial rectus recession when compared with bilateral medial rectus recession in 29 patients who developed consecutive large angle esotropia after bilateral lateral rectus recession for intermittent exotropia. It is not common in the clinical practice that a bilateral lateral rectus muscle recession for exotropia results in an overcorrection; in any case in this study, there is no comparison with bilateral advancement of the operated lateral rectus muscles, which seems to be the most rational approach to restoring the original condition without operating virgin muscles or creating any incomitance. Some recent studies introduce a new possible pathogenesis and definition of distance esotropia in the elderly. It is proposed that small-angle esotropia or hypertropia may result from involutional changes in extraocular muscles and orbital connective tissues, in particular a symmetrical or asymmetrical lateral rectus sag and lateral rectus-superior rectus band rupture that configures a ‘‘sagging eye syndrome’’ or an age-related distance esotropia.86Y89 Prism correction may be proposed to treat this condition, but good results can be obtained by means of a surgical loop myopexy on the slipped lateral rectus muscle.

Exotropia An interesting review from the Cochrane Database on interventions for intermittent exotropia has been published.90 The authors found only 1 randomized study by Kushner in 199890 showing unilateral surgery to be more effective than bilateral lateral rectus recession for the intermittent basic type of exotropia. As mentioned previously about the literature on interventions for infantile esotropia, this review also highlights some limitations, in particular the many different approaches to the management of exotropia that are proposed with a lack of certainty regarding the most effective treatment(s) and surgical timing. In a study by Hatt et al,91 an important role of parental health-related life quality in the decision on performing surgery in intermittent exotropia is underlined. In particular, children with intermittent exotropia whose accompanying parent was reported to have poorer health-related life quality were more likely to undergo surgery than those whose accompanying parent was reported to have better health-related life quality. This suggests that the role of parental educational or counseling interventions should be explored. * 2014 Asia Pacific Academy of Ophthalmology

Pattern Strabismus With regards to pattern strabismus, Ghasia and Shaikh92 propose 2 different pathogenetic mechanisms. Abnormal neural connections maybe responsible for the development of pattern in infantile-onset strabismus. The loss of fusion would cause a torsional drift responsible for an alteration of the pulling direction of recti muscles. Probable anomalies in supranuclear circuits not yet identified with certainty would be present. Bilateral brainstem lesions would cause a decreased anterior semicircular canal input responsible for an imbalance between the tone of the superior oblique and inferior oblique muscles. On the other hand, orbital pulley instability and abnormal static torsion maybe responsible for the development of pattern in late-onset strabismus and craniofacial anomalies. With regards to the surgical treatment, there is a lack of certainty regarding the most effective treatment(s), in particular the effectiveness of the oblique muscles surgery and that of vertical transposition of recti muscles.92 We plan a surgical procedure of a recession of the oblique muscles only in the presence of their overaction. Action on the rectus muscles is indicated in the absence of oblique muscles dysfunction.

Cranial Nerves Palsy With regards to the sixth cranial nerve palsy, an easy and fast surgical procedure is described in a retrospective study on only 9 patients. It is a scleral fixation of vertical recti 10 to 12 mm from the limbus.93 A prospective study presents a very complicated surgical procedure for complete third cranial nerve palsy with 50% of stable results and 50% of undercorrection or no change in vertical deviation.94 Transposition procedures, lateral rectus fixation, and globe anchoring procedures are well reviewed and explained in the study by Sadagopan and Wasserman.95

Duane Syndrome Encouraging results after surgery are described with Fosteraugmented vertical recti transposition in Duane syndrome type 1 and sixth cranial nerve palsy in terms of deviation, anomalous head posture, and binocular single visual field.96 We think that a fundamental role is probably played by preoperative motility, in particular the residual abduction, which is not always detectable before surgery. As regards Duane syndrome type 2, a prospective study with short follow-up on lateral rectus periosteal fixation compared with additional partial vertical recti transposition in exo-Duane syndrome shows good results for both techniques but little improvement in adduction and binocular single visual field with additional vertical recti transposition.97 As regards Duane syndrome type 3, in the study by Snir et al,98 a contralateral lateral rectus muscle recession for the treatment of moderate unilateral Duane syndrome type 3 is proposed, with motor and functional improvement and decrease in head turn. Good results with inferior oblique myectomy are described in very selected cases of Duane syndrome with upshoot.99 Furthermore, some reports on associations between Duane syndrome and other diseases and genetic alterations are present in the literature, but the numbers are small, and the available data do not allow definitive conclusions.

Brown Syndrome In an interesting study by Kaeser and Brodsky,100 an intriguing pathogenetic theory is proposed. Brown syndrome resulting from primary structural abnormalities, the classical form, can go toward a potential spontaneous improvement related either to natural growth or to the repetitive elevation of the eye induced by the contraction of the superior rectus muscle. On the www.apjo.org


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contrary, dysinnervational Brown syndrome, demonstrable by clinical and neuroimaging evidence, persists throughout life.

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ocular misalignment, but also for reduced social anxiety levels that may be associated with improvements in their quality of life and disability levels.108

Surgery An interesting study by Shin et al101 demonstrates that Ztenotomy of superior oblique up to 50% progressively reduces extraocular tendon force transmission, but when greater than 50%, it is biomechanically equivalent, in vitro, to complete tenotomy.101 Yang et al102 investigated the use of fibrin glue for closure of conjunctival incision in strabismus surgery. Less postoperative inflammation and shorter operating time are described, but an increased percentage of wounds requiring subsequent repair with sutures is reported.102 Neither cost-effectiveness nor risk of viral transmission was evaluated. In a study by Ludwig et al,103 surgical techniques are exhaustively described. They suggest some options of approaching difficult strabismus problems. In particular, the authors describe the correction of consecutive strabismus attributable to stretched scar, the pulley posterior fixation procedure to correct high accommodative convergence or to augment a maximal medial rectus recession, the repair of the partial avulsion of a rectus muscle for the correction of restrictive strabismus, the nasal myectomy of the inferior oblique muscle to correct persistent inferior oblique overaction, and the full advancement of the superior oblique tendon as an option to strengthen a weak superior oblique muscle. Rabinowitz et al104 investigated the risk factors influencing the outcome of strabismus surgery after retinal detachment surgery with scleral buckle and confirmed that small preoperative deviations and minimally restricted ocular rotations were associated with better outcomes of strabismus surgery and that removing the scleral buckle did not improve results. An interesting review from the Cochrane Database on a comparison between adjustable versus nonadjustable sutures for strabismus has been published.105 The authors found only 1 prospective study by Tripathi in 2003,105 demonstrating better results with adjustable sutures. However, there was no description of patients who showed undercorrection, nor was there any description of patients with complete information on the profile of cases and controls (dysthyroidism). In general, no agreement on accuracy of long-term ocular alignment is present in the literature, and there is no agreement on whether a particular technique is superior in specific situations. Visuomotor control after surgical correction of strabismus in adults was investigated in a study by Sharan.106 No significant impact of strabismus surgery in adulthood on the control of visually guided actions was found, probably because compensatory strategies had been used continuously. However, the study had a small number of patients (only 3) with no data about stereopsis in the preoperative period. The follow-up is rather short with a maximum of 12 months.

Strabismus and Quality of Life There is a recent study by Bagheri et al107 which demonstrates that the total IQ is significantly lower in patients with congenital strabismus, and that lower IQ levels are associated with coexisting amblyopia. The question concerns the presence of a genetic background rather than the role of acquired causes.107 A very recent study by Alpak et al108 investigates the effects of corrective surgery on strabismus patients in terms of the presence of a diagnosis of social phobia, their severity of social anxiety symptoms, disease-related disability, and their quality of life. The authors conclude that adult strabismus patients seem to benefit from corrective surgery not only for their

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A good leader can engage in a debate frankly and thoroughly, knowing that at the end he and the other side must be closer, and thus emerge stronger. You don’t have that idea when you are arrogant, superficial, and uninformed. V Nelson Mandela


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