British Journal ofOphthalmology 1992; 76: 723-727

Refraction changes in children developingconvergent or divergent strabismus

Maths Abrahamsson, Gerhard Fabian, Johan Sjostrand

AbstractStrabismus and amblyopia were studied in acohort of children born in 1979 or 1980 in thearea of Viisterias, Sweden. Forty percent of thechildren had participated in a voluntary eyeexamination at 1 year of age. All childrendiagnosed as strabismic and/or amblyopicbetween 1979 and 1988 at any of the three eyeclinics in the area were included in this study.Strabismic cases were mostly detected by theparents while microstrabismus and straighteye amblyopia were found at the general 4years of age screening at children's healthcentres. In 57 cases with (n=31) and withoutamblyopia (n=41) it was possible to obtainseveral refraction values between 1 and 6 yearsof age. In this study we concentrated onmanifest esotropia and exotropia. The aim ofthe study was to describe changes of refractionbefore and after onset of strabismus and toestablish risk indicators that identifiedpopulations at risk of developing strabismus.We found that patients with esotropia show amore pronounced hypermetropia thanexotropic cases at the time of detection ofstrabismus. This difference becomes moredefinite over time, since hypermetropiaincreased in the deviating eye in the esotropiccases while refractive errors remainedstationary in most of the exotropic eyes. It wasalso apparent that anisometropia frequentlydeveloped after onset of strabismus in eso-tropic cases in contrast to exotropic cases. Anincreasing refractive error in the deviatingesotropic eye could be combined with anemmetropisation of the fixating eye.(BrJ7 Ophthalmol 1992; 76: 723-727)

Department ofOphthalmology,University of Goteborg,SwedenM AbrahamssonG FabianJ SjostrandCorrespondence to:Dr Maths Abrahamsson,Department ofOphthalmology, S-413 45Goteborg, Sweden.Accepted for publication22 July 1992

During the past two decades there has been a

focus of interest on the changes of refractionduring infancy and childhood. Previously it wasbelieved that infants were hypermetropic at birthand that there was a decrease in hypermetropiaduring infancy and childhood. Later it was

determined that as many as 20% of the newbornare myopic. Other studies have shown thatafter the infantile period (at 1 or 2 years of age)most children are hypermetropic.'3 From theage of approximately 1 year there is a decrease inrefractive errors, especially in the amount ofastigmatism.3-5 These data together with otherstudies indicate that there are considerablechanges in refraction during the first years oflifei. -8One reason for this growing interest is the

possibility of using refractive errors as riskindicators useful in screening programmes foryoung children in order to prevent amblyopiaand squint. Knowledge of potentially dangerous

refractive anomalies is necessary in order todefine the population at risk. The high variabilityof the individual refraction during early child-hood complicates the determination of riskindicators. Age becomes an essential factor forevaluation ofwhen a refraction error is potentiallydetrimental for visual development.

In- this study we were interested in therefractive changes of children who developstrabismus. In patients with convergentstrabismus we have known that there is arelationship to hypermetropia since 1864 whenDonders presented his publication 'On theanomalies of accommodation and refraction ofthe eye.' This has later been confirmed by severalstudies (cf Duke Elder).9 The longitudinalchanges of refraction in esotropic individualshave also been studied,"'-'2 and one study hasexamined refractive changes before the onset ofstrabismus." Though these studies9-" all found ahigh hyperopia in most cases with esotropia it isstill difficult to determine a refraction limit atany particular age that separates potentiallyesotropic children from normal ones.

In divergent strabismus, early studies byDonders indicated an association with myopia.This relationship was questioned however at thebeginning of this century.9 There seems to be aportion of myopia among the exotropic childrenbut the majority are hypermetropic at onset.The aim of this study was to compare refraction

changes in children with manifest esotropia orexotropia compared with the development of therefractive errors in normal children. We alsowanted to examine refractive changes before andafter the onset of the strabismus to detectwhether abnormal refractive behaviour could beused as an indicator for pointing out patients atrisk of developing strabismus and/or amblyopia.

Methods

SUBJECTSRefraction data for the study were obtained bycombining two different studies. In the first weexamined, motility, fixation, refractive errors,and heredity of 9000 children at 1 year of age.These children took part in a voluntary ophthal-mic examination (1971-81). The examinationwas offered through children's health carecentres to all children in the city of Vasteras,Sweden. Approximately 50% of the childrenborn in the area took part in the examination.

In the second study we scrutinised the hospitalfiles of all children born between 1979 and 1980who visited one of the three ophthalmic clinics inthe city of Vasteras, Sweden, during the 1980s.We found 715 cases that for some reason visitedan eye clinic before 8 years of age. There were a

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Table I Distribution ofstrabismus

Esotropia Exotropia Microtropia Infantile Paralytic Total

Number of patients 41 21 8 6 4 80Percentage of strabismic

patients 51 26 10 8 5 100Percentage of all children

born in the area 79, 80 1-4 0 7 0-3 0-2 0-1 2-7

large variety of reasons for the visits. Mostcommon were conjunctivitis, trauma, strabis-mus, or suspected amblyopia. In 290 of thesepatients we have refraction data from the volun-tary examination at 1 year of age that could beanalysed together with data from the first visit toan eye clinic. In 57 cases with strabismus (n= 31)and/or amblyopia (n=41) it was possible toobtain a series ofrefraction values between 1 yearof age and up to 5 or 6 years of age.The patients were refracted by retinoscopy 30

minutes after instillation of cyclopentolate (1%).Spectacles were prescribed at detection of thestrabismus in patients with hypermetropia-2D. The anisometropia of the strabismic andamblyopic patients was fully corrected. None ofthe amblyopic and/or strabismic cases worespectacles before detection of strabismus/amblyopia. Time of detection was defined as thedate when strabismus is diagnosed by anophthalmologist or by an orthoptist.

In this study we describe refraction andrefraction changes and their significance inpatients with manifest strabismus. The reliabilityof the data depends on the accuracy of therefraction data and ability of the screeningprogramme to detect patients with amblyopiaand strabismus and refer them to an eye clinic. Inour earlier studies all refraction determinationshave been done by one ophthalmologist (GF)with much experience of refraction determi-nation in young children.I'3''4 All refractionmeasurements with young children wereperformed by GF while some refraction data inolder children were obtained from several otherophthalmologists at different eye clinics. We areaware of the problem of having several ophthal-mologists involved and have tried to minimisethe effects.We have chosen to follow longitudinal changes

in refraction from 1 to 4 years in the majority ofcases. The reason for choosing 4 years as anendpoint is that we have a general healthscreening in Sweden at the age of 4 years. Morethan 95% of all children take part in thatscreening. Studies indicate that most amblyopic

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Figure I The age at whichamblyopia is diagnosed byan ophthalmologist at an eyeclinic in the city of Vasterds,Sweden, is presentedfor allchildren born in 1979 or1980. The hatched columnsindicate those children withamblyopia identified by thescreening programme atapproximately 4 years ofage.

cn 20cn0)

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Age (years)

cases that are not previously known are identifiedat this screening.'5 6

STRABISMUS AND AMBLYOPIAThe cases of manifest strabismus (n= 80) wereclassified into one of five categories; esotropia,exotropia, microstrabismus, infantile, andparalytic strabismus (Table 1). Infantile strabis-mus was defined as a manifest strabismusdetected before 9 months of age. All patientswith predominantly intermittent strabismuswere excluded from the study. We concentratedespecially on the cases with esotropia andexotropia. The cases with infantile esotropia andmicrostrabismus were not included in thecomparison of refraction changes (Figures 4 and5).

Straight eye amblyopia and microstrabismusare generally detected by the Swedish generalhealth screening'5 and cases with strabismus arereferred to an eye clinic by the children's healthcare centres. Children with monocular visualacuity lower than 0 8 or an interocular differencein acuity of two rows or more (HVOT ortumbling E letter chart) at the 4 year screeningare retested within the screening programme.Children with subnormal vision at both these testsessions are referred to an eye clinic. We havechosen to use a somewhat uncommon definitionof amblyopia in our analysis of the hospital files.A patient must fulfil the following two criteria inorder to be classified as amblyopic: (1) an acuitydifference (approximately 0 -I log unit or more,which equals 1 line or more) between the eyesmeasured at the eye clinic with best correction atleast two separate consecutive test sessions ineyes with no signs of disease; (2) the acuity of the'amblyopic' eye improved at least one linefollowing the occlusion treatment.The first criterion means that a child will have

his visual acuity tested four times before he orshe is classified as amblyopic if referred from thegeneral health screening programme. Childrenreferred from sources outside the screeningprogramme pass two visual acuity tests or morebefore they are classified as amblyopic. Theamblyopic cases (n= 126) were classified into

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Age (years)Figure 2 The age at which strabismus is diagnosed by anophthalmologist is presentedfor all children born in 1979 or1980 and visiting an eye clinic in the city ofVasterds, Sweden.In the diagram both manifest and intermittent strabismus areincluded. The hatched columns indicate those children withstrabismus (mainly microstrabismus) identified by thescreening programme at approximately 4 years ofage.

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Refraction changes in children developing convergent or divergent strabismus

Figure 3 The relativedistribution ofthe age atdetection ofcases withmanifest strabismus ispresentedfor children withesotropia and exotropiarespectively. The column 0-1year contains only casesdetected between 9 and 12months ofage.

30 -

25 -

20-

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15-a)

10-

5-

ESO

EXO

0-<1 1-<2 2-<3 3-<4 4-<5 .5Age (years)

three different groups according to the severityof the visual loss. The best corrected visualacuity (VA) of the amblyopic eye at the start oftreatment was graded in three levels as follows:VA -0 2, 0 2<VA.0 5, and VA >0 5.

ResultsIn Swedish children there are different patternsfor detection of strabismus compared withamblyopia. Cases with amblyopia without eyedeviation or with microstrabismus are mostlyidentified by the visual screening programme.All (>95%) of the Swedish children have ageneral health examination, including an eyeexamination, at 4 years ofage. In Figure 1 the ageat detection ofamblyopia is presented. The casesidentified earlier than 4 years of age usually havelarge angle strabismus or amblyopia caused byvisual deprivation (that is, infantile cataract,ptosis). The detection pattern of strabismus isdifferent (Fig 2). The age of detection is evenlydistributed between 1 and 4 years. The screeningprogramme identifies undetected microstrabis-mic cases while cases with manifest large anglestrabismus are identified by the parents. Thesecases are referred by the children's health centreto an ophthalmologist shortly after onset of thestrabismus. In Table 1 the distribution of thedifferent types of manifest strabismus ispresented both as numbers and as a percentage of

Figure 4 The refractionerrorfor the deviating eye atthe age ofdetection ispresented for children withmanifest esotropia andexotropia respectively. Sincethe anisometropia waspresent in approximately10% ofthe cases therefractive error ofthefixingeyes is approximately thesame as the refractiveerror ofthe deviating eye.

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patients found in hospital files, and as a percent-age of all children born in the area. Approxi-mately 75% of all cases with strabismus wereclassified as exotropia or esotropia. Infantile,paralytic, and microstrabismus representedapproximately one quarter of all strabismusdiagnoses. The ratio between number of caseswith convergent and divergent strabismus wasapproximately 2: 1.

REFRACTION AND REFRACTION CHANGESFor the study of refraction we have concentratedour analysis of the refraction changes with timein cases with manifest esotropia and exotropia(n=62, Table 1). No cases of infantile strabismus(detected earlier than 9 months of age), paralyticstrabismus, microstrabismus, or predominantlyintermittent strabismus were included. The ageat detection of the two types of strabismus ispresented in Figure 3. The onset of esotropia andexotropiais distributed differently. Most (:95%)esotropic cases are detected between 1 and 4years ofage while more than 40% of the exotropiccases are detected later than 4 years of age.At the time of detection of strabismus,

astigmatism (-1-0 D) is common (29% of allcases) in both eyes in both convergent anddivergent strabismus while anisometropia ismore uncommon in both esotropia and exotropia(esotropia n=5/41; exotropia n=3/21). Thedistribution of the refractive error (sphericalequivalent) in the deviated eye at detection,however, is different between the two groups ofstrabismus (Fig 4). More than 60% of theesotropic patients have a hypermetropia that ismore than 2 dioptres in the deviating eye at thedate of detection while we found no case withmyopia in this group. It is notable that in seven(18%) of the esotropic cases the refractive errorwas less than 1 dioptre in any meridian. Inexotropia larger refraction errors are more

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<-1 -1-<O O-< 1 1-<2 2-3Refractive changes (dioptres)

Figure 5 The longitudinal changes in refraction of thedeviating eye ofchildren with manifest esotropia and exotropiarespectively. The refraction changes are calculated as sphericalequivalent at 4 years ofage minus spherical equivalent at Iyear ofage.

<-1 0-<1 2-<3 4-<5-1-<O 1-<2 3-<4 5-<6

Refractive errors (dioptres)

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Table 2 Distribution ofamblyopia

VA-0-2 02<VA-05 05<<VA Total

Number of patients 11 46 69 126Percentage of amblyopic

patients 8-7 36-5 54 8 100Percentage of all childrenborninthearea79,80 0-3 1 5 2-3 4-1

uncommon. In 65% of the cases the errors arebetween -1 and +2 D in the deviating eye. Oneexotropic patient has a pronounced myopia(- 8 D) in both eyes.

In order to study differences of refractiveerrors in the deviating eye at onset two agegroups were compared: children younger than36 months at onset (but older than 9 months) andolder than 36 months. No significant differencein the distribution of refractive error in con-vergent or divergent squint respectively could befound for the two age groups. The same differ-ences between exotropia and esotropia asdescribed above were thus found in both agegroups.The refractive changes between 1 and 4 years

of age could be studied in 23 cases with non-

alternating strabismus, 14 esotropic (14/41), andnine exotropic (9/21) patients (Fig 5). At 1 year ofage one esotropic and two exotropic patients are

myopic and five esotropes and three exotropeshad a hypermetropia greater or equal to 3 5 D inthe most hypermetropic meridian in any eye.The majority of the esotropic patients (10/14)show an increase in hypermetropia :0 5 D in thestrabismic eye during the period from 1 to 4years. Increasing hyperopia could be identifiedboth before and after the detection of the eso-tropia in more than 50% of the deviating eyeswhile in several cases there was an emmetropisa-tion or at least a decreasing hypermetropia in thefixating eye. In the esotropic patients aniso-metropia developed owing to this difference inbehaviour between the eyes. At 1 year of age aswell as at onset ofthe esotropia there is one (1/14)case with anisometropia. One year after onset(11-16 months) 13 ofthe esotropes had developedanisometropia greater or equal to 1 D. Mostpatients with divergent squint showed small(c0-5 D) or no changes in the refraction ineither eye (7/9). The same process of developinganisometropia as in convergent squint couldnot be seen.

STRABISMUS AND AMBLYOPIAThe distribution of acuity of all amblyopic eyes ispresented in Table 2. We used the amblyopiadefinition presented in the Methods section andclassified the patients into different groupsaccording to the severity of the visual loss. Inmore than 50% of the cases with amblyopia thevisual acuity in the amblyopic eye was betterthan 0 5. When we combine the distributions ofamblyopia and strabismus (Tables 1 and 2) in thewhole population we found that in our estimationof distribution 2-7% of all children hadstrabismus and 4-2% had amblyopia, while thepercentage with both amblyopia and strabismuswas 1-4%.Amblyopia was present in 53% of all the cases

with manifest strabismus (42/80) while patientswith squint represented 33% of all amblyopiccases (42/126). When we study only severeamblyopia (VA <0 2) the relationship betweenamblyopia and strabismus is much morepronounced: 72% of the patients with severeamblyopia were also squinting (8/11). The distri-bution of convergent and divergent strabismusinto different amblyopia categories was verysimilar. Approximately 20% in both groups ofstrabismus developed severe amblyopia(VA <0 2). The same was true for microstrabis-mus while all cases of paralytic strabismuspresented with amblyopia of a low magnitude(VA >0 5). The number of patients is small sothese data can suffer from random errors.The treatment for amblyopia was unsuccessful

in six cases out of 80 (7 5%) with strabismus.Unsuccessful means a difference in acuity of tworows or more after the conclusion ofthe occlusiontreatment. Five of the cases who remainedamblyopic despite treatment had convergentsquint, and in only one case was a divergentsquint present. That child also had nystagmus.Among the five children with esotropia andamblyopia persisting after treatment two caseshad severe amblyopia.

DiscussionThere is a limited knowledge of the causes ofmanifest squint. However, in some cases thegeneral mechanisms that produce the squint areknown. Brain damage, neuromuscularanomalies, and abnormalities of the fusionmechanism are related to motor problems thatcan cause squint. Strabismus can also be causedby mechanical factors in the orbit. Finally thereis an established relationship between accom-modation, refraction, and concomitant squint.Several studies have pointed out that hyper-metropia and anisometropia are overrepresentedin cases with convergent squint." 12 In our studywe found that almost two thirds of the esotropeshad hypermetropia (spherical equivalent) - thatis, over 2 D in the deviating eye - whereas only7% had anisometropia at onset. The relationshipbetween hyperopia and esotropia is mostprobably causal in many of the cases. There is aplausible aetiological connection throughaccommodation and the strabismus may be curedby correcting the refraction error.The relationship between ametropia and the

development of strabismus is discussed in mosttextbooks. Both anisometropia and hyper-metropia, as well as pronounced astigmatism,have been said to trigger the development ofstrabismus owing to disturbances of fusion.More recent studies'7 have pointed outmeridional hypermetropia of +335 or more in achild at 1 year of age as a useful risk indicatorboth for amblyopia and strabismus. In our studywe found that five of 14 cases with esotropia hada hypermetropia of +335 or more at 1 year ofage. This number has increased to seven of 14esotropes at onset of the strabismus. The con-nection between age and refractive error hasproved to be ever more interesting, since there isa high variability and change in refraction duringthe first years of life.' 3 ' lX" In earlier studies we

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Refraction changes in children developing convergent or divergent strabismus

found that in certain cases more than 4 dioptresof astigmatism and anisometropia may disappearduring the period 1 of 4 years.313 14

In this study we found that most of thechildren before onset of their convergent squinthad a hypermetropia of >2 D or more in thedeviating eye at 1 year of age while it wasuncommon with hypermetropia -2 D at thesame age in the deviating eye in cases with futuredivergent squint. In a normal control eye therefractive error should have decreased to 1-1 5 Dat the age of4 years. Studying the refractive errorat 4 years we found a very limited decrease inrefraction of the deviating eye of both groups(Fig 5). Among the convergent squinters therewas even an increase in the refractive error inmost cases, with as much as 2 75 D in one case. Ifesotropia was characterised by an increasingrefractive error divergent squint was charac-terised by a lack of emmetropisation of thedeviating eye. In most of the exotropic casesthere was no change in refraction at all during thetest period of 1 to 4 years.A most interesting finding was that some

esotropic cases developed anisometropia afterthe onset of the strabismus. Seven percent of theesotropes had anisometropia at onset whichcould be compared with the 10% we found forthe whole population at that age level'3 (andunpublished data). Among the 14 esotropic caseswhich could be followed with respect to refractionbetween 1 and 4 years one case had aniso-metropia at onset of strabismus. At 1 year after(11-16 months) onset 13 of 14 children haddeveloped anisometropia. This tendency todevelop anisometropia following onset inesotropic patients can also be seen in otherstudies of longitudinal changes in refraction inthe deviating eye before and after onset ofstrabismus.'01" In our study anisometropia wasfound in all but one case ofconvergent strabismusat 1 year after the onset of the squint. Detailedstudy of the refractive changes indicates that theanisometropia is created owing to the fact thatthe fixating eye is emmetropising, while thisprocess is interrupted in the deviating eye. Weeven found increasing refractive errors in thedeviating eye. Data from Aurell and Norrsell"indicate disturbances in the emmetropisationprocess in both eyes before the onset of theesotropia in children with a family history ofstrabismus. Since our data are collected withouta specific time schedule for the testing it isimpossible to calculate any mean difference intime between the onset of strabismus and theonset of anisometropia. Among the patients withdivergent squint no case could be demonstratedwith anisometropia developing after the onset ofthe squint.

In a study of the relationship betweenrefraction and amblyopia'4 we found that anincreasing refractive error between 1 and 4 yearsof age was related to the development ofamblyopia in cases without deviation. The sameseems to be true for the development of con-vergent strabismus. In this study we found thatno child developed esotropia which had adecreasing refraction in the deviating eye beforeonset. Development of esotropia without aniso-

metropia at onset was the most common finding.After onset we found cases with anisometropiaand esotropia without amblyopia but no casewith amblyopia and esotropia without aniso-metropia among those cases longitudinallyfollowed. It is known that one can have aniso-metropia and amblyopia without esotropia.From those findings one may conclude that bothesotropia and amblyopia are strongly associatedwith anisometropia; the combination of theseparticular conditions has the potential to causeanisometropia.

In divergent squint refraction seems to beneither a cause nor a risk indicator. We found norelationship between refraction and refractionchanges and the development of divergentstrabismus.

In conclusion, there is evidence thatconvergent and divergent squint are caused bydifferent mechanisms. Refraction changesbetween 1 and 4 years of age characterised byfailure of emmetropisation are observed both incases developing convergent strabismus oramblyopia without any deviation. Anisometropiais mainly a secondary phenomenon in conver-gent squint while it can be a primary condition indivergent squint.

This study was supported by Swedish Medical Research Council(grant 02226), Handianden H Svensson foundation, the DBVassociation, and the first of May flower annual campaign forchildren's health. We are grateful to the staff at the Eye Clinic atCentrallasarettet, Herrgardets Virdscentral and Vastra Sjukhusetin the City of Vasteras. Finally, we will also thank Ann-KatrinAndersson and orthoptist Eileen Bentley for their invaluablesupport.

1 Fabian G, Wendell ME. Ophthalmological and orthopticexamination of 1200 children up to age 2. AmOrthoptJ 1974;24: 86-90.

2 Goldschinidt E. Refraction of the newborn. Acta Ophthalmol(Kbh) 1969; 47: 570-8.

3 Abrahamsson M, Fabian G, Sjostrand J. Changes in astig-matism between the ages of 1 and 4 years: a longitudinalstudy. BrJ Ophthalmol 1986; 92: 145-9.

4 Atkinson J, Braddick 0, French J. Infant astigmatism: itsdisappearance with age. Vison Res 1980; 20: 891-3.

5 GwiazdaJ, Scheiman M,MohindraI. Astigmatism in children:changes in the axis and amount from birth to 6 years. InvestOphthalmol Vis Sci 1984; 25: 88-92.

6 Slapater FJ. Age norms of refraction and vision. Arch Ophthal-mol 1950; 43:466-81.

7 Hirsch MJ. Refraction in children. AmJ Optom 1964; 41:395-9.

8 Ingram RM, Barr A. Changes in refraction between the ages ofland 3-5 years. BrJ Ophthalmol 1979; 63: 339-42.

9 Duke-Elder S, Wybar K. Ocular motility and strabismus.System of Ophthalmology. S Duke-Elder, ed. 15 vols.London: Henry Kimpton, 1973; VI: 577-641.

10 Lepard CW. Comparative changes in the error of refractionbetween fixing and amblyopic eyes during growth anddevelopment. AmJ Ophthalmol 1975; 80:485-90.

11 Aurell E, Norrsell K. A longitudinal study of children with afamily history of strabismus: factors determining theincidence of strabismus. BrJ Ophthalmol 1990; 74: 589-94.

12 Otsuka J, Sato Y. Supplementary study of comparison ofrefractive components of orthophoric hyperopic eyes withthose of accommodative esotropic eyes. Acta Soc OphthalmolJpn 1984; 88: 58-64.

13 Abrahamsson M, Fabian G, Sjostrand J. A longitudinal studyof a population based sample of astigmatic children. II. Thechangeability of anisometropia. Acta Ophthalmol (Kbh)1990; 68:435-40.

14 Abrahamsson M, Fabian G, Andersson A-K, Sjostrand J. Alongitudinal study of a population based sample of astigmaticchildren. I. Refraction and amblyopia. Acta Ophthalmol(Kbh) 1990; 68:428-34.

15 Kohler L, Stigmar G. Vision screening of four-year-oldchildren. Acta PaediatrScand 1973; 62: 17-27.

16 Kohler L, Stigmar G. Visual disorders in 7-year-old childrenwith and without previous vision screening. Acta PaediatrScand 1978; 67: 373-7.

17 Ingram RM, Walker C, Wilson JM, Arnold PE, Dally S.Prediction of amblyopia and squint by means of refractive atage one year. BrJr Ophthalmol 1986; 70: 12-5.

18 Fulton AB, Dobson Y, Salem D, Mar C, Petersen RA, HansenRM. Cycloplegic refraction in infants and young children.AmJr Ophthalmol 1980; 90: 239-47.

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