tonic accommodation, age, and refractive error in children

11
Tonic Accommodation, Age, and Refractive Error in Children Karla Zadnik, 1 Donald 0. Mutti, 1 ' 2 H. S. Kim, 5 Lisa A. Jones, 4 Pei-Hua Qiu, 4 and Melvin L Moeschberget 5 PURPOSE. An association between tonic accommodation, the resting accommodative position of the eye in the absence of a visually compelling stimulus, and refractive error has been reported in adults and children. In general, myopes have the lowest (or least myopic) levels of tonic accommodation. The purpose in assessing tonic accommodation was to evaluate it as a predictor of onset of myopia. METHODS. Tonic accommodation was measured in children enrolled in the Orinda Longitudinal Study of Myopia using an infrared autorefractor (model R-l; Canon, Lake Success, NY) while children viewed an empty litfieldor a darkfieldwith afixationspot projected in Maxwellian view. Children aged 6 to 15 years were measured from 1991 through 1994 (n = 714, 766, 771, and 790 during the 4 years, successively). Autorefraction provided refractive error and tonic accommoda- tion data, and videophakometry measured crystalline lens curvatures. RESULTS. Comparison of the two methods for measuring tonic accommodation shows a significant effect of age across all years of testing, with the lit empty-field test condition yielding higher levels of tonic accommodation compared with the dark-field test condition in children aged 6 through 11 years. For data collected in 1994, mean (±SD) tonic accommodation values for the lit empty-field condition were significantly lower in myopes, intermediate in emmetropes, and highest in hyper- opes (1.02 ± 1.18 D, 1.92 ± 1.59 D, and 2.25 ± 1.78 D, respectively; Kruskal-Wallis test, P < 0.001; between-group testing shows each group is different from the other two). Age, refractive error, and Gullstrand lens power were significant terms in a multiple regression model of tonic accommodation (R 2 = 0.18 for 1994 data). Lower levels of tonic accommodation for children entering the study in thefirstor third grades were not associated with an increased risk of the onset of myopia, whether measured in the lit empty-field test condition (relative risk = 0.90; 95% confidence interval = 0.75, 1.08), or the dark-field test condition (relative risk = 0.83; 95% confidence interval = 0.60, 1.14). CONCLUSIONS. This is the first study to document an association between age and tonic accommo- dation. The known association between tonic accommodation and refractive error was confirmed and it was shown that an ocular component, Gullstrand lens power, also contributed to the tonic accommodation level. There does not seem to be an increased risk of onset of juvenile myopia associated with tonic accommodation. (Invest Ophthalmol Vis Set. 1999;40:1050-1060) T onic accommodation is the resting position of the ac- commodative system in the absence of compelling vi- sual stimuli. It is generally reported to have a range of 0.50 D to 4.00 D, with a mean of approximately 1.50 D in adults. 1 Tonic accommodation and its adaptation (how it changes after active accommodation) have attracted consider- able interest in recent years as a putative risk factor for myo- pia 2 ' 3 and have been studied widely as a function of refractive error. 45 In early studies, it was shown that emmetropes had significantly higher (i.e., more myopic) values of tonic accom- From the 'College of Optometry; the 'College of Medicine and Public Health, Division of Epidemiology and Biometrics; and the ''Bio- statistics Program, The Ohio State University, Columbus; and the 2 School of Optometry, University of California, Berkeley. Supported by Grant EY08893 from the National Institutes of Health, Bethesda, Maryland. Submitted for publication February 3, 1998; revised November 30, 1998; accepted January 20, 1999. Proprietary interest category: N. Reprint requests: Karla Zadnik, The Ohio State University College of Optometry, 338 West Tenth Avenue, Columbus, OH 43210-1240. modation than did high myopes. 6 Later, distinctions were drawn within the subgroup of myopia, and hyperopes were examined. Juvenile-onset myopes and emmetropes had similar tonic accommodation values, whereas hyperopes had higher tonic accommodation values, and adult-onset myopes had lower tonic accommodation values. 7 Similar relations have been shown in children, with tonic accommodation values progressing from highest in hyperopes, to intermediate in emmetropes, to lowest in juvenile-onset myopes. 8 ' 9 Shifts in tonic accommodation of brief duration have been shown during and after near-work tasks, and these short-term shifts seem to vary by refractive error category. Sustained visual work at near increased tonic accommodation immediately after the task (i.e., tonic accommodation shifted in the myopic direction) in those with adult-onset myopia, whereas hyper- opes showed decreases in tonic accommodation. Little change in tonic accommodation was exhibited by juvenile-onset myopes and emmetropes after sustained near work. 10 In one study, all children increased in tonic accommodation after playing video games, with juvenile-onset myopes showing the 1050 Investigative Ophthalmology & Visual Science, May 1999, Vol. 40, No. 6 Copyright © Association for Research in Vision and Ophthalmology

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Tonic Accommodation, Age, and Refractive Error inChildren

Karla Zadnik,1 Donald 0. Mutti,1'2 H. S. Kim,5 Lisa A. Jones,4 Pei-Hua Qiu,4 andMelvin L Moeschberget5

PURPOSE. An association between tonic accommodation, the resting accommodative position of theeye in the absence of a visually compelling stimulus, and refractive error has been reported in adultsand children. In general, myopes have the lowest (or least myopic) levels of tonic accommodation.The purpose in assessing tonic accommodation was to evaluate it as a predictor of onset of myopia.

METHODS. Tonic accommodation was measured in children enrolled in the Orinda LongitudinalStudy of Myopia using an infrared autorefractor (model R-l; Canon, Lake Success, NY) whilechildren viewed an empty lit field or a dark field with a fixation spot projected in Maxwellian view.Children aged 6 to 15 years were measured from 1991 through 1994 (n = 714, 766, 771, and 790during the 4 years, successively). Autorefraction provided refractive error and tonic accommoda-tion data, and videophakometry measured crystalline lens curvatures.

RESULTS. Comparison of the two methods for measuring tonic accommodation shows a significanteffect of age across all years of testing, with the lit empty-field test condition yielding higher levelsof tonic accommodation compared with the dark-field test condition in children aged 6 through 11years. For data collected in 1994, mean (±SD) tonic accommodation values for the lit empty-fieldcondition were significantly lower in myopes, intermediate in emmetropes, and highest in hyper-opes (1.02 ± 1.18 D, 1.92 ± 1.59 D, and 2.25 ± 1.78 D, respectively; Kruskal-Wallis test, P <0.001; between-group testing shows each group is different from the other two). Age, refractiveerror, and Gullstrand lens power were significant terms in a multiple regression model of tonicaccommodation (R2 = 0.18 for 1994 data). Lower levels of tonic accommodation for childrenentering the study in the first or third grades were not associated with an increased risk of the onsetof myopia, whether measured in the lit empty-field test condition (relative risk = 0.90; 95%confidence interval = 0.75, 1.08), or the dark-field test condition (relative risk = 0.83; 95%confidence interval = 0.60, 1.14).

CONCLUSIONS. This is the first study to document an association between age and tonic accommo-dation. The known association between tonic accommodation and refractive error was confirmedand it was shown that an ocular component, Gullstrand lens power, also contributed to the tonicaccommodation level. There does not seem to be an increased risk of onset of juvenile myopiaassociated with tonic accommodation. (Invest Ophthalmol Vis Set. 1999;40:1050-1060)

Tonic accommodation is the resting position of the ac-commodative system in the absence of compelling vi-sual stimuli. It is generally reported to have a range of

0.50 D to 4.00 D, with a mean of approximately 1.50 D inadults.1 Tonic accommodation and its adaptation (how itchanges after active accommodation) have attracted consider-able interest in recent years as a putative risk factor for myo-pia2'3 and have been studied widely as a function of refractiveerror.45 In early studies, it was shown that emmetropes hadsignificantly higher (i.e., more myopic) values of tonic accom-

From the 'College of Optometry; the 'College of Medicine andPublic Health, Division of Epidemiology and Biometrics; and the ''Bio-statistics Program, The Ohio State University, Columbus; and the2School of Optometry, University of California, Berkeley.

Supported by Grant EY08893 from the National Institutes ofHealth, Bethesda, Maryland.

Submitted for publication February 3, 1998; revised November 30,1998; accepted January 20, 1999.

Proprietary interest category: N.Reprint requests: Karla Zadnik, The Ohio State University College

of Optometry, 338 West Tenth Avenue, Columbus, OH 43210-1240.

modation than did high myopes.6 Later, distinctions weredrawn within the subgroup of myopia, and hyperopes wereexamined. Juvenile-onset myopes and emmetropes had similartonic accommodation values, whereas hyperopes had highertonic accommodation values, and adult-onset myopes hadlower tonic accommodation values.7 Similar relations havebeen shown in children, with tonic accommodation valuesprogressing from highest in hyperopes, to intermediate inemmetropes, to lowest in juvenile-onset myopes.8'9

Shifts in tonic accommodation of brief duration have beenshown during and after near-work tasks, and these short-termshifts seem to vary by refractive error category. Sustained visualwork at near increased tonic accommodation immediately afterthe task (i.e., tonic accommodation shifted in the myopicdirection) in those with adult-onset myopia, whereas hyper-opes showed decreases in tonic accommodation. Little changein tonic accommodation was exhibited by juvenile-onsetmyopes and emmetropes after sustained near work.10 In onestudy, all children increased in tonic accommodation afterplaying video games, with juvenile-onset myopes showing the

1050Investigative Ophthalmology & Visual Science, May 1999, Vol. 40, No. 6Copyright © Association for Research in Vision and Ophthalmology

IOVS, May 1999, Vol. 40, No. 6 Tonic Accommodation and Refractive Error 1051

greatest increase.9 Tonic accommodation has been shown toincrease during tasks involving cognitive demand as well.11'12

Tonic accommodation has been measured in many ways.With all methods, the goal is to measure the resting state ofaccommodation under open-loop conditions. The method var-ies by laboratory and investigator, and individual laboratorieshave generally adopted a favored method. The methods usedinclude measurement with the Badal helium-neon laser op-tometer while viewing laser-produced speckles on a rotatingcylindrical drum,113 infrared optometry while the subjectviews a dark field6'4"'7 or a lit empty field,17 autorefractionwhile the subject views a dark field,7'9"'3 and dynamic (Nott)retinoscopy while the subject views the retinoscopic beam'3

or a difference of Gaussian target.818

Tonic accommodation has been reported to be more my-opic by approximately 0.50 D when measured in a lightedempty field compared with that measured in the dark.'9 In asubsequent study, investigators using procedures similar tothose in the present study found no significant differencesbetween resting measures of pretask tonic accommodation inempty-field conditions and in darkness.17

Three studies comparing methods in adults have beenpublished, one comparing subjective and objective methods inthe form of helium-neon laser optometry, infrared optometry,and near (dynamic) retinoscopy13; one comparing adaptationof tonic accommodation with infrared autorefraction whileviewing either a dark or lit empty field17; and one comparingdynamic retinoscopy viewing either a difference of Gaussiantarget or the retinoscope beam.20 In the first study, resultswere similar for all three measurement methods, although nearretinoscopy showed less variability across subjects.13 In thesecond study, tonic accommodation levels were not affectedby whether the subjects viewed a dark field or lit empty fieldwhile tonic accommodation was measured with an infraredautorefractor.l7 In the third, the results show that tonic accom-modation measured in the dark differs from tonic accommo-dation measured under other conditions for a variety of rea-sons.20 To date, different test conditions and measurementmethods for tonic accommodation in children have not beencompared.

The relation between tonic accommodation and the ocu-lar components has not been explored beyond that reportedfor refractive error. For example, the possibility that a person'sor a refractive error group's tonic accommodation levels maybe a consequence of crystalline lens shape and power has notbeen considered previously. Correlation coefficients betweenrefractive error and tonic accommodation have ranged from0.6l,2 to 0.48,6 to 0.24.7 In two studies, investigators haveperformed regression analysis on tonic accommodation versusrefractive error,8'9 but none has made comparisons with any ofthe anatomic ocular components.

Our purpose in measuring tonic accommodation in theOrinda Longitudinal Study of Myopia (OLSM) from 1991through 1994 included several objectives. First, we wanted tocompare measurement methods in school-aged children. Sec-ond, we wanted to verify the previously reported relationbetween tonic accommodation and refractive error in ourOLSM sample. Third, we wanted to determine the associations,if any, between tonic accommodation and the ocular compo-nents, especially those relating to the crystalline lens. Finally,we wanted to evaluate tonic accommodation as a risk factor forthe onset of myopia in children.

TABLE 1. Children Enrolled in the Orinda LongitudinalStudy of Myopia, 1991 through 1994

Age*

6789101112131415Total

1991

48100839489728190525

714

Year Tested

1992

491301007690908493522

766

1993

431391159577828675563

771

1994

5711212412292698184490

790

Children represented in this table had both lit empty-field anddark-field measures of tonic accommodation at each measurementoccasion.

* By age rounded to the nearest year.

METHODS

SubjectsThe study design and entire sample for the OLSM have beendescribed previously.21 All children enrolled in the OrindaUnion School District in grades 1,3, and 6 in fall 1989 or fall1990; in grades 1 or 6 in fall 1991; or in grade 1 in fall 1992,1993, or 1994 were eligible for this phase of the study. Parentsgave consent for their children's participation after all studyprocedures were explained in accordance with the tenets ofthe Declaration of Helsinki. The subjects from the OLSM rep-resented in this report are all children measured from 1991through 1994 for whom we have tonic accommodation mea-sures for fixation of the empty lit field and the dark field, asdescribed later (n = 714, 766, 771, and 790 in the 4 years,successively). All children measured from 1991 through 1994in the OLSM are included. Children enrolled in or before 1991had the potential to be represented in the data set four times,children enrolled in 1992 were represented in the data setthree times, children enrolled in 1993 were represented in thedata set twice, and children enrolled in 1994 were representedin the data set once. Age at the time of testing was rounded tothe nearest year (e.g., 14.6 through 154 years was coded as 15years for the purposes of data analysis). The number of subjectsin each age group for children measured in each of the 4 yearsis shown in Table 1.

MeasurementRefractive error was measured by noncycloplegic autorefrac-tion (model R-l; Canon, Lake Success, NY; no longer manufac-tured). Subjects had the left eye occluded by an eye patchwhile viewing the 6/9 (20/30) equivalent row of letters on areduced Snellen card through a +4.00 D Badal lens. Subjectiverefraction techniques were simulated in this apparatus by mov-ing the letter target along a track away from the subject to relaxaccommodation, as though plus lenses were being added.Readings were recorded at the point at which the target wasclear, and any movement to relax accommodation furtherresulted in the subject's reporting blur. At least 10 readings

1052 Zadnik et al. IOVS, May 1999, Vol. 40, No. 6

were taken on the right eye. Spurious values were eliminatedaccording to a previously described protocol.21

We measured the right eye's ocular components and re-fractive error in the subject sample as described previously indetail.21 Specifically, we used the autorefractor to measurerefractive error, the photokeratoscope (KERA; Fremont, CA;no longer manufactured) to measure corneal power, videophakometry to measure crystalline lens curvatures,22 and anultrasound scanning unit (model 820 A-scan; Humphrey, SanLeandro, CA) to measure the eye's axial dimensions, anteriorchamber depth, crystalline lens thickness, and vitreous cham-ber depth.23 Although measurement of the various compo-nents was divided among three examiners, each examinermeasured the same components on each subject at each an-nual session.

Topical agents were used to induce corneal anesthesia(0.5% proparacaine), pupillary mydriasis, and cycloplegia (twodrops of 1.0% tropicamide administered 5 minutes apart). Non-cycloplegic refractive error, corneal power, and tonic accom-modation were measured before drop instillation. Cycloplegicrefractive error, crystalline lens curvatures, and axial dimen-sions were all measured beginning 25 minutes after the firstdrop of tropicamide. We have previously documented theeffectiveness of tropicamide as a cycloplegic agent in a com-parable sample of children.24'25 All measurements were con-ducted without examiner knowledge of the child's visual ac-tivity profile or parental history of myopia.

For the purposes of refractive error classification, childrenwere categorized on the basis of the right eye's cycloplegicautorefraction in the vertical and horizontal meridians (averageof 10 readings)26 as follows: Myopes were defined as having atleast —0.75 D of myopia in the vertical and horizontal merid-ians, hyperopes had at least +1.00 D of hyperopia in thevertical and horizontal meridians, and emmetropes repre-sented the rest of the sample.

Measurement of Tonic AccommodationLit Empty Field. A translucent plate of polypropylene

was placed over the examiner's side of the mirror housing onthe autorefractor. Edges of the housing were obscured by asecond polypropylene plate placed on the patient's side of themirror housing. This plate contained a rectangular aperture (30mm X 95 mm). The edges of this aperture were further ob-scured by strips of translucent cellophane tape on each edge,making a final aperture size of 25 mm X 75 mm (20° X 56°).Testing took place in a converted 34-ft mobile home trailerparked out of doors. The autorefractor was located in a roomlit by natural light from one window. Lighting conditions weretherefore variable depending on the time of day and weatherconditions (50-100 candela[cd]/m2). Supplemental illumina-tion from a fluorescent fixture was directed at the polypro-pylene plate during late afternoon testing times or overcastconditions. Children were instructed to look toward the mid-dle of the plate as though they were looking out a window tokeep their fixation centered in the autorefractor. The left eyewas occluded by an eye patch. The examiner held up a fingerin the middle of the plate to direct fixation. Once the childshowed that he or she understood where to look, the fingerwas removed, and readings were taken.

Some young children were unable to maintain steadyfixation in the absence of stimuli. To obtain data from all theyounger subjects, children in first and second grades fixated a

15% contrast smudge consisting of a circle 8 mm in diameter(5°) drawn on a piece of translucent cellophane tape andattached to the plate on the examiner's side. The polypro-pylene plates and autorefractor mirror were regularly cleanedof dust and other particles.

Dark Field with Fixation Light. We also measured tonicaccommodation in modified darkness. Room lights remainedon while the subject wore a pair of custom sunglasses contain-ing an opaque lens over the left eye and a Wratten 89B infraredfilter over the right eye. This filter transmits only wavelengthslonger than 680 nm. The autorefractor possesses sufficientsensitivity to infrared light to make measurements through thisfilter. Room lighting was visible around the edges of the sun-glasses. The infrared illumination lights on the autorefractorwere covered by a removable mask to create a dark fieldcentrally. Steady fixation in darkness was made possible byprojecting a red spot in Maxwellian view in the middle of thedark field. This fixation spot was produced by placing a 0.5 mmdiameter pinhole illuminated by an incandescent source at thefocal point of a +6.25 D lens. A second +6.25 D lens imagedthis pinhole in the pupillary plane of the right eye of eachsubject. The pinhole was frosted with translucent tape toobscure any detail of the filament of the light source. Thelateral extent of the fixation spot was restricted by placing a 3mm aperture 20 mm from the pinhole.

At least 10 autorefractor readings were recorded in theright eye by each method by the same examiner. The order ofmeasurement was determined by a random number table. Newsequences were used for each year of testing. The data were"scrubbed" by identifying sphere values on the autorefractorprintout for a subject that differed from his or her median valueby at least 5.00 D. High initial values were discarded if readingsdecreased by 3-00 D or more. Readings were also discarded ifaccompanied by a cylinder axis differing significantly from themode axis (e.g., by 80°). Readings were not discarded if vari-ation in tonic accommodation occurred randomly within a setof readings, as opposed to systematically decreasing from ahigh initial value. The mean sphere from the lit empty-field anddark-field conditions was subtracted from the mean spherefrom the noncycloplegic autorefraction to yield the values oftonic accommodation used in the following analyses.

Statistical MethodsThe data set collected from the OLSM was analyzed cross-sectionally and longitudinally in separate analyses to examinethe factors associated with tonic accommodation. The out-come variables were tonic accommodation measured by theempty-field method and by the dark-field method, as describedearlier. The explanatory variables were age, cycloplegic refrac-tive error, and other ocular components: corneal power, ante-rior chamber depth, lens thickness, Gullstrand lens power,calculated equivalent lens power, lens equivalent refractiveindex, calculated lens spherical volume,27 vitreous chamberdepth, and axial length. First, the cross-sectional analysis wasperformed for data collected in 1991, 1992, 1993, and 1994.Analysis of variance was used to determine whether tonicaccommodation was different among refractive error groups(myope, emmetrope, and hyperope) and whether it was re-lated to age. Second, if data were not approximately normallydistributed, then the nonparametric Kruskal-Wallis one-wayanalysis of variance was used. Groups were further comparedby Wilcoxon rank sum tests if the Kruskal-Wallis test was

IOVS, May 1999, Vol. 40, No. 6 Tonic Accommodation and Refractive Error 1053

3.50

1991 1992

7 8 9 1 0 1 1 1 2 1 3 1 4Age (years)

0.50 - -I 1-

6 7 8 9 1 0 1 1 1 2 1 3 1 4Age (years)

1 9 9 3

3.50

1 9 9 4

6 7 8 9 1 0 1 1 1 2 1 3 1 4Age (years)

6 7 8 9 1 0 1 1 1 2 1 3 1 4Age (years)

FIGURE 1. A plot of tonic accommodation as a function of age for both viewing conditions, lit empty field(dashed line) and dark field (solid line), as a function of the children's age for each of the 4 years of testing.

significant. Multiple regression with a stepwise selection pro-cedure was used to select statistically significant explanatoryvariables. Because children of the same age across the 4 yearswere not the same children, the data were independent by ageacross test years. The independence of cross-sectional dataallowed data across the 4 years to be combined by age. Third,the repeated measure design was used with longitudinal datameasured in children who entered into OLSM only in schoolgrades 1,3, and 6 to determine the cohort and/or time effectsfor tonic accommodation. The statistical analysis software pro-gram (Statistical Analysis System; SAS, Cary, NC) was used forcross-sectional data analysis,28 and another procedure (BMDP-5V; BMDP, Berkeley, CA) was used for the repeated measuresanalysis because of its capability for handling missing values.29

Relative risks for the occurrence of myopia were obtainedfrom a proportional hazards time-to-event analysis.30 In thepresent study, the time variable was the length of time thechildren were under observation, and either they became my-opic or the study concluded without their becoming myopic.This model customarily assumes that the hazards (or risks) forvarious levels of a factor are proportional. The assumption ofproportional hazards was verified. All children in this analysiswere nonmyopic at enrollment. Time to myopia was modeledusing tonic accommodation under each test condition as co-variates. Analyses were completed separately for children en-

rolled in the study during the first, third, or sixth grades, andfor all children who were tested in the third grade, regardlessof their grade at entry. (This included children enrolled in firstgrade who were eventually tested during third grade.)

RESULTS

The tonic accommodation values for both viewing conditions,lit empty field and dark field with fixation light, as a function ofthe children's age are shown in Figure 1 (cross-sectional data).Across all 4 years when these data were collected in the samechildren, it is evident that the lit empty-field condition yieldedsignificantly higher tonic accommodation values in youngerchildren compared with the dark-field test condition. Thisdifference is therefore unlikely to be caused by a cohort effectof children tested in any 1 year. The differences disappearbetween ages 9 and 14 years. These differences are againevident in Figure 2A, in which the data are collapsed across testyears (cross-sectional data). It is apparent from Figure 2B thatthe 95% confidence intervals for the difference between thetonic accommodation data for the lit empty-field and the dark-field test conditions do not include 0 through age 11 years,indicating statistically significant differences between results ofthe two test conditions through that age.

1054 Zadnik et aJL IOVS, May 1999, Vol. 40, No. 6

3.50

0.00

8 9 10 1 1 1 2 13 14 15

Age (years)

B8 9 1 0 1 1 1 2 1 3 14 15

Age (years)

FIGURE 2. A plot of tonic accommodation versus age (A) for all datacollected from 1991 through 1994 under the lit empty-field test con-dition and the dark-field test conditions. The difference in tonic ac-commodation (B) under the two test conditions as a function of age,with the 95% confidence interval depicted for each age group.

As an estimate of the repeatability of the tonic accommo-dation measurement techniques, we randomly selected 50 chil-dren tested in both 1990 and 1991 whose refractive errorcategories had not changed between testing occasions. Giventhat their tonic accommodation would be expected to changeslightly with increasing age (Fig. 1), we found an interoccasionmean difference in the lit empty-field measurement of 0.03 ±1.39 D and an interoccasion mean difference in the dark-fieldwith fixation light measurement of —0.07 ± 1.54 D. Althoughthese values did not represent a high degree of repeatability(95% limits of agreement of ±2.72 D and ±3.02 D, respec-tively) of this obviously "noisy" measure in children, the pre-viously reported relation between tonic accommodation andrefractive error was still evident (Fig. 3), an indication of themeasurement method's robustness and validity.

The relation between refractive error and tonic accommo-dation across age groups is represented in Figure 3 (cross-sectional data). In all age groups, myopes showed the lowest

value of tonic accommodation, with emmetropes and hyper-opes in general showing higher values of tonic accommoda-tion.

The data for tonic accommodation under both viewingconditions are shown in Table 2 by refractive error group forall 4 years of data (cross-sectional data). The relation betweenrefractive error and tonic accommodation was evident withboth measurement methods across the years of the study. Forthe lit empty-field test condition, the levels of tonic accommo-dation were different among the refractive error groups(Kruskal-Wallis test; P < 0.001). Myopes had the lowest levelsof tonic accommodation, emmetropes the intermediate levels,and hyperopes the highest levels (Wilcoxon rank sum test:myopes compared with emmetropes, P < 0.001; myopes com-pared with hyperopes, P < 0.001; and emmetropes comparedwith hyperopes, P < 0.023). For the dark-field test condition,the levels of tonic accommodation were also different amongthe refractive error groups (Kruskal-Wallis test, P < 0.001).However, only the myopes were different; the emmetropesand hyperopes were statistically equivalent (Wilcoxon ranksum test: myopes compared with emmetropes, P < 0.001;myopes compared with hyperopes, P < 0.001; and em-metropes compared with hyperopes, P = 0.765).

The results of multiple, stepwise regressions to determinethe effect of age, refractive error, and the ocular componentson tonic accommodation under the lit empty-field and thedark-field viewing conditions are shown in Tables 3 and 4(cross-sectional data). All variables in Tables 3 and 4 representthose that were screened as significant at P = 0.15 level by astepwise multiple regression selection method. For tonic ac-commodation under the lit empty-field viewing condition (Ta-ble 3), age, refractive error, and Gullstrand lens power wererepresented in the models of all 4 years' data. Calculated lenspower contributed minimally to the model in 2 years, as didcorneal power in 1 year. Anterior chamber depth, lens thick-ness, and lens spherical volume all entered the model in only 1year, 1994.

For tonic accommodation under the dark-field viewingcondition (Table 4), the picture was much less consistentacross years. Gullstrand lens power was significant across all 4years, refractive error was significant in 3 of the 4 years' datasets, and age was significant in 2 of the 4 years. Axial length,corneal power, and corneal curvature entered the model in astatistically significant way in only 1 year each. Overall, the R2

values across years for tonic accommodation with the dark-field viewing condition were lower than those for tonic accom-modation with the lit empty-field viewing condition, indicatingthat, in general, much less of the variability in the former couldbe explained by age, refractive error, and the ocular compo-nents.

Thus, in Table 5 we have chosen to highlight tonic ac-commodation with the lit empty-field viewing condition.Across the years, multiple regression analyses on tonic accom-modation with the lit empty-field viewing condition show thatthe important and consistent predictor variables were age,refractive error, and Gullstrand lens power. The results ofmultiple regression modeling on tonic accommodation withonly these three variables in the model are shown.

In an attempt to exploit the statistical power of longitudi-nal analyses and the ability to construct independent age sam-ples from longitudinal data, repeated measures analyses forchildren entered into OLSM in school grades 1,3, and 6 were

IOVS, May 1999, Vol. 40, No. 6 Tonic Accommodation and Refractive Error 1055

1991 1992

10-

•I 6ro

! A\

8 2 •< n

y

I °-2

if3 144 35M E HAge 6-7

12 ,

10

8

6 •

4 •

2

0

- 2 •

-4

12

0

0 °

• •

• •

3 113 32

M E HAge 6-7

1993

• o

.II•4 155 18

M E HAge 8-9

0

f

ill• ; :• •

f

si*• o

(Number of subjects)23 127 11 41 173 14

M E HAge10-11

M E HAge>=12

11 172 27(Number of subjects)

10 140 9 45 162 13

M E HAge 8-9

M E HAge10-11

M E HAge>= 12

12

10

.< 8

(0

li6 140 33

M E HAge 6-7

1994

3 134 32

M E HAge 6-7

9 139 28

M E HAge 8-9

ii si11 205 30M E HAge 8-9

il(Number of subjects)

19 154 7 44 172 15

M E HAge10-11

M E HAge>=12

o (Number of subjects)13 131 17 33 174 7

M E HAge10-11

M E HAge >= 12

FIGURE 3. Box plots for tonic accommodation under the lit empty-field viewing condition as a function of age and refractive error for each testyear. The open box represents the median value; the upper and lower ends of the filled rectangles the 75th and 25th percentiles, respectively; andthe upper and lower filled circles the 100th and zero percentiles, respectively, after excluding outliers. The open circles represent outlying valuesdiffering from the nearest value by at least 1.00 D.

performed (Table 6). In each analysis, there was a significantinteraction term between the cohort enrolled in 1989 and theinitial measurement time, which was controlled for in the

analysis. Changes in refractive error, Gullstrand lens power,and crystalline lens refractive index were all significant inmodeling the change in tonic accommodation in children

TABLE 2. Tonic Accommodation by Refractive Error Group for Data Collected in 1991 through 1994

YearRefractive

Error Group

MyopesEmmetropesHyperopes

MyopesEmmetropesHyperopes

MyopesEmmetropesHyperopes

MyopesEmmetropesHyperopes

Number ofSubjects

7156875

7860583

6961884

6064486

Tonic Accommodationwith Lit, Empty Field

1.05 ± 0.762.13 ± 1.712.26 ± 1.92

1.20 ± 1.292.13 ± 1.692.40 ± 2.27

1.10 ± 0.992.15 ± 1.742.21 ± 1.83

0.79 ± 0.781.92 ± 1.592.46 ± 1.88

Tonic Accommodationwith Dark Field

1991

1992

1993

1994

0.94 ± 0.831.70 ± 1.501.77 ± 1.83

1.00 ± 1.401.71 ± 1.582.06 ± 2.09

0.93 ± 1.061.75 ± 1.611.41 ± 1.55

1.07 ± 1.431.70 ± 1.631.63 ± 1.63

Tonic accommodation under both viewing conditions is significantly lower in myopes and is different across refractive error groups under thelit empty-field condition for all years of the study. Data are means ± SD in diopters.

1056 Zadnik et al. IOVS, May 1999, Vol. 40, No. 6

TABLE 3. Multiple Stepwise Regression Results for Tonic AccommodationMeasured under the Lit Empty-Field Viewing Condition

Year

1991

1992

1993

1994

Variable

AgeRefractive errorGullstrand lens power

AgeGullstrand lens powerCorneal powerRefractive errorCalculated lens power

AgeGullstrand lens powerRefractive errorCalculated lens power

AgeRefractive errorGullstrand lens powerAnterior chamber depthLens thicknessLens spherical volume

Coefficient

-0.1300.2100.139

-0.1830.287

-0.1190.111

-0.058

-0.1480.2110.112

-0.066

-0.2250.1450.069

-0.414-6.128

0.070

Partial R2 P

0.075 0.00010.026 0.00010.013 0.0012Adjusted R2 = 0.109

0.106 0.00010.028 0.00010.011 0.00190.007 0.01490.002 0.1488Adjusted R2 = 0.148

0.096 0.00010.018 0.00010.006 0.02510.004 0.0660Adjusted/?2 = 0.121

0.158 0.00010.016 0.00010.008 0.00740.003 0.11190.004 0.05210.003 0.0839Adjusted/?2 = 0.184

All variables included in this table represent those that were "screened" as significant at P < 0.15.

enrolled as first graders. Only refractive error and Gullstrandlens power were significant in those enrolled as third graders;and only refractive error, Gullstrand lens power, and anteriorchamber depth are significant in those enrolled as sixth grad-ers. These results confirm those of the cross-sectional analysesin that the terms that emerge most consistently as explanatoryof tonic accommodation, although they explain a very small

portion of its variance, are Gullstrand lens power and cyclo-plegic refractive error.

Despite the association between a child's current refrac-tive error and tonic accommodation, it does not seem to be astatistically significant risk factor for the future onset of myo-pia. Relative risks for tonic accommodation by both methodswere calculated from a proportional hazards time-to-event

TABLE 4. Multiple Stepwise Regression Results for Tonic AccommodationMeasured under the Dark-Field with Fixation Light Viewing Condition

Year

1991

1992

1993

1994

Variable

Axial lengthCorneal powerGullstrand lens power

Gullstrand lens powerRefractive errorAgeCorneal power

Gullstrand lens powerRefractive errorCalculated lens power

AgeGullstrand lens powerRefractive error

Coefficient

-0.335-0.092

0.087

0.2140.134

-0.062-0.059

0.2400.115

-0.067

-0.0720.1070.084

Partial R2 P

0.037 0.00010.008 0.01570.005 0.0613Adjusted R2 = 0.046

0.050 0.00010.019 0.00010.007 0.01960.003 0.1072Adjusted i?2 = 0.073

0.046 0.00010.008 0.00990.005 0.0547Adjusted i?2 = 0.056

0.023 0.00010.007 0.01560.004 0.0651Adjusted i?2 = 0.0297

All variables included in this table represent those that were "screened" as significant at P < 0.15-

IOVS, May 1999, Vol. 40, No. 6 Tonic Accommodation and Refractive Error 1057

TABLE 5. Tonic Accommodation under the Lit Empty-Field Viewing ConditionModeled across Years with Multiple Regression Models Containing Only Age,Refractive Error, and Gullstrand Lens Power

Year

1991

1992

1993

1994

Variable

AgeRefractive errorGullstrand lens power

AgeRefractive errorGullstrand lens power

AgeRefractive errorGullstrand lens power

AgeRefractive errorGullstrand lens power

Coefficient

-0.1300.2100.139

-0.1730.1240.211

-0.1530.1060.161

-0.2320.1620.161

Partial R2 P

0.032 0.00010.024 0.00010.015 0.0013Adjusted R2 = 0.110

0.054 0.00010.010 0.00520.030 0.0001Adjusted R2 = 0.139

0.038 0.00010.008 0.01480.021 0.0001Adjusted R2 = 0.118

0.109 0.00010.020 0.00010.010 0.0060Adjusted/?2 = 0.177

analysis30 with the onset of myopia (at least —0.75 D in bothprincipal meridians) as the event. The time variable is thelength of time until each child either became myopic or thestudy concluded without the child becoming myopic, for chil-dren enrolling in OLSM in the first, third, or sixth grades, or forchildren enrolling in the first or third grades, with third gradedata serving as the baseline (Table 7; longitudinal data). Therelative risks for tonic accommodation were not statisticallysignificant, regardless of grade at enrollment or measurementmethod used.

DISCUSSION

These results showing tonic accommodation under two view-ing conditions in school-aged children represent the largestdata set ever assembled of tonic accommodation in any agegroup. We found an age-related difference between tonic ac-commodation measurements made under the two viewingconditions: a lit empty field and a dark field with fixation light.We also found the first association reported between increas-

ing age and less myopic levels of tonic accommodation. Weconfirmed the frequently reported association between tonicaccommodation and refractive error,4 "y regardless of viewingcondition. When ocular components were included with re-fractive error in a regression analysis, we also found a compa-rably modest but significant association between Gullstrandlens power and tonic accommodation.

Studies of tonic accommodation provide support for ac-commodative theories of refractive error development.31

Along with the development of animal models of myopia, thetonic accommodation studies of the 1980s are in large partresponsible for the renaissance of interest in the study ofhuman myopia that the field currently enjoys. To date, theinterpretation of tonic accommodation data has been that thevariability in tonic accommodation and its adaptation reflectsthe differences in autonomic balance in the eye and thereforemay play a role in the causation of refractive error. A theoryconnecting autonomic status and tonic accommodation describestonic accommodation as the balance point between the sympa-thetic and parasympathetic components of accommodation.32

TABLE 6. Unbalanced Repeated Measures Multiple Regressions of Cohort Number (1991 through 1994), Time ofMeasurement, Refractive Error, and the Ocular Components on Tonic Accommodation Measured Under the LitEmpty-Field Test Condition

Grade atEnrollment

1

3

6

Number ofSubjects

430

182

256

Variable

Refractive errorGullstrand lens powerLens refractive index

Refractive errorGullstrand lens power

Anterior chamber depthRefractive errorGullstrand lens power

Coefficient

0.1570.150

20.488

0.1130.156

-0.6450.0920.092

SE

0.0530.0447.102

0.0560.049

0.2990.0470.047

P

0.00300.00070.0039

0.04500.0003

0.03070.04770.0491

1058 Zadnik et al. IOVS, May 1999, Vol. 40, No. 6

TABLE 7. Relative-Risk Tonic Accommodation and Onset of Juvenile Myopia for Children Enrolled in the OLSM

GradeEnrolled

113661 or 31 or 3

Tonic AccommodationTest Condition

Lit empty fieldDark fieldLit empty fieldLit empty fieldDark fieldLit empty fieldDark field

Number ofSubjects

667491174217

70558384

Relative Risk

0.82(0.66, 1.01)0.95 (0.73, 1.24)0.81 (0.62, 1.04)0.72(0.48, 1.08)0.48(0.17, 1.35)0.90(0.75, 1.08)0.83(0.60, 1.14)

P

0.0580.7250.0960.1110.1640.2680.250

The grade in the table represents the grade at enrollment. All prevalent myopes were excluded from this analysis, and incident cases of myopiadeveloped after the subject enrolled. Incident myopes were defined as those with at least —0.75 D of myopia on cycloplegic autorefraction in bothmeridians. Note: No baseline data are available for tonic accommodation tested under the dark-field test condition for children enrolled in the thirdgrade in either 1989 or 1990. Values in parentheses are 95% confidence intervals.

Further connection between autonomic tone and refractionwas proposed by van Alphen,33 who thought that centrallycontrolled ciliary muscle and choroidal tension could modifythe effects of intraocular pressure and thus control refractivedevelopment.

Little attention has been paid to the question of whetherthe differences in tonic accommodation by refractive errorstatus are perhaps a consequence of refractive status ratherthan a cause of differences in refractive status. These datasupport the interpretation of tonic accommodation as either aconcomitant change with or a consequence of refractive error,rather than as a cause. It seems that the relation betweenGullstrand lens power and tonic accommodation (Tables 3, 4,5) supports the idea that a particular crystalline lens anatomy,the flatter radii characteristic of myopia, is associated with aless myopic tonic accommodation level. Whereas van Alphen33

proposed that an increase in ciliary tension, assumed to bereflected in higher values of tonic accommodation, would beprotective against the expansion of the eye, we propose thatincreased ciliary tension resulting from ocular expansionstretches and flattens the crystalline lens, producing lowerlevels of tonic accommodation. In support of this association ofcrystalline lens anatomy with tonic accommodation, crystallinelens thinning during the period in which children are suscep-tible to juvenile-onset myopia has been described.34 Loss in thepower of the crystalline lens during the school years is associ-ated with lens curvature flattening and a decrease in lens-equivalent index.35 Mechanical forces on the lens resultingfrom equatorial growth that accompanies axial growth of theeye may explain these results. If these equatorial stretchingforces in the larger, myopic eye increase ciliary tension on thecrystalline lens, it is entirely conceivable that the lens willassume a less powerful position under open-loop conditions,producing lower tonic accommodation levels. The absence ofany significant association between tonic accommodation andthe risk of future myopia further supports the view that thelower levels of tonic accommodation seen in myopes are aconsequence rather than a cause of juvenile-onset myopia.

A report of tonic accommodation levels just before theinception of adult-onset myopia also found that low levels oftonic accommodation accompany, but do not precede, theonset of myopia.36 Another investigator reports high tonicaccommodation in emmetropes who become myopes, but thesmall sample size, use of an inappropriate parametric statistic,

and failure to correct for multiple comparisons make thismarginally significant result inconclusive at best.37

The differences between the two test conditions, espe-cially the differences in the younger children, raise the ques-tion of which test condition represents "truth." We incorpo-rated the dark-field test condition specifically to avoid some ofthe proximal effects inherent in the lit empty-field test condi-tion, but inspection of the data in Tables 3 and 4 shows thatboth conditions explained variability in tonic accommodationby differences in refractive error and Gullstrand lens power.Perhaps the more rigorous, less contaminated dark-field testcondition failed to capture important variance occurring withtonic accommodation and age in school-aged children. Studiesin small samples of children in which various open-loop con-ditions are used could help sort out this question.

The greater difference in tonic accommodation betweenmethods in the younger subjects could be caused by thefixation smudge used to maintain accurate fixation in the firstand second grade children. We think this is unlikely. The8-year-olds (no smudge condition) were no different from the6 year-olds (Fig. 2; smudge test condition). In Figure 3, therelation shown between tonic accommodation and refractiveerror is the same for 6- to 7-year-olds as for any other age group.Both of these points argue against the sudden removal of somecontaminating factor after second grade (6- and 7-year-olds)that affected either the absolute value of tonic accommodation,its relation with refractive error, or our ability to evaluate it asa predictive factor for onset of myopia. In addition, the age-related difference between the lit empty-field and the dark-fieldwith fixation light test conditions persisted well beyond the 6-and 7-year-old age groups in which the difference in testcondition was not an issue.

Accommodative adaptation is another potential confound-ing factor. Before measurement of tonic accommodation, chil-dren were wearing their habitual refractive error correction (orwere not). Children are not monitored in the OLSM specificallyfor compliance with wear of their correction, although wehave noted that children wear their glasses more sporadicallythan eye care practitioners might like to think. Some myopeshad their correction on before testing, perhaps all morning.This would represent different numbers of hours depending onwhether they were tested as our first or last group of the schoolday. Others may have put their glasses on just before proceed-ing to the mobile clinic. Many moderate hyperopes have no

IOVS, May 1999, Vol. 40, No. 6 Tonic Accommodation and Refractive Error 1059

correction. Thus, the precise level of accommodative stimulusand therefore adaptation before testing is not known.

Adaptation effects reported in children virtually eliminatethe association between tonic accommodation and refractiveerror.9 This raises the question of whether the nonsignincanceof tonic accommodation as a risk factor for the onset of myopiain children may be the result of adaptation effects. Threearguments may be made against this causal relation. First,obvious adaptation was eliminated when high initial tonicaccommodation readings were discarded. Second, prolongedadaptation effects are measured in the laboratory during main-tained open-loop conditions—that is, closing the eyes andmaintaining a dark environment,9 extinguishing a lit target,3 ormaintaining pinholes in Maxwellian view.38 It is not knownhow periods of closed-loop distance fixation may interruptadaptation. Ebenholtz3 reported that distance fixation may bemore powerful in creating adaptation, thereby reducing tonicaccommodation, than near fixation may be in increasing tonicaccommodation. The walk from the classroom to the testingsession may serve as a "washout" period for adaptation effects.Finally, the finding of an association between tonic accommo-dation and refractive error by both methods argues againstadaptation effects reducing our ability to detect different levelsof tonic accommodation in children in whom myopia devel-oped later.

In summary, we found an association between tonic ac-commodation and refractive error. Myopes had the lowestvalues of tonic accommodation in both test conditions, andhyperopes had the highest values of tonic accommodation inthe lit empty-field test condition. Tonic accommodation de-creased with increasing age, especially when measured withthe lit empty-field test condition. Tonic accommodation mea-sured under the lit empty-field test condition was approxi-mately 0.75 D greater than tonic accommodation measuredunder the dark-field test condition between the ages of 6 and11 years.

Multiple regression models using age, refractive error, andGullstrand lens power accounted for little of the variance intonic accommodation under the lit empty-field test conditionand even less in tonic accommodation under the dark-fieldcondition. Gullstrand lens power was the anatomic, ocularcomponent most strongly associated with tonic accommoda-tion. Tonic accommodation by either method failed to predictthe onset of juvenile myopia. These data support the conceptthat tonic accommodation is probably a consequence of devel-oping refractive error, rather than a cause.

Acknowledgment

The authors thank Nina E. Friedman and Pamela A. Qualley, Universityof California, Berkeley School of Optometry, for their assistance, andMark A. Bullimore, The Ohio State University College of Optometry, foradvice.

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