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Height, Stunting, and Refractive Error Among Rural ChineseSchoolchildren: The See Well to Learn Well Project

ABHISHEK SHARMA, NATHAN CONGDON, YANG GAO, YAOGUI LU, YANRU YE, JING WU,DENNIS S. C. LAM, LIPING LI, JIASI WU, YEE KIT TSE, MINGZHI ZHANG, YUE SONG, AND

SIAN GRIFFITHS

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PURPOSE: To evaluate the hypothesis that changes inutritional status could be partly responsible for observed

ncreases in myopia prevalence among Chinese children.DESIGN: Cross-sectional cohort study.METHODS: Rural Chinese secondary school children

articipating in a study of interventions to promotepectacle use were randomly sampled (20% of childrenith uncorrected vision >6/12 bilaterally, and 100% of

emaining children) and underwent cycloplegic refrac-ion with subjective refinement and measurement ofeight and weight. Stunting was defined according to theorld Health Organization standard population.RESULTS: Among 3226 children in the sample, 2905

90.0%) took part. Among 1477 children undergoingefraction, 1371 (92.8%) had height and weight mea-urements. These children had a mean age of 14.5 � 1.4ears, 59.8% were girls, and mean spherical equivalentefraction was �1.93 � 1.82 diopters. Stunting wasresent in 87 children (6.4%). While height was in-ersely associated with refractive error (RE) (tallerhildren were more myopic) among boys (r � �0.147,

� .001), this disappeared when adjusting for age, ando such association was observed among girls. Neitherirls nor boys with stunting differed significantly inefraction from children without stunting, and neithertunting nor height was associated with RE when adjust-ng for age, height, and parental education. The power ofhis study to have detected a 0.75 diopters difference inE between children with and without stunting was.96.CONCLUSION: Results from this cross-sectional study

re not consistent with the hypothesis that nutritionaltatus is a determinant of RE in this setting. (Am Jphthalmol 2010;149:347–353. © 2010 by Elsevier

nc. All rights reserved.)

ccepted for publication Aug 13, 2009.From the Oxford University Department of Public Health, Oxford,nited Kingdom (A.S.); Chinese University of Hong Kong Department

f Ophthalmology and Visual Sciences, Hong Kong, China (N.C.,.S.C.L.); Joint Shantou International Eye Center of Shantou University

nd Chinese University of Hong Kong, Shantou, China (N.C., Jin.W.,.S.C.L., Jia.W., M.Z., Y.S.); Chinese University of Hong Kong Schoolf Public Health, Hong Kong, China (Y.G., Y.K.T., S.G.); and Shantouniversity Faculty of Medicine, Shantou, China (Y.L., Y.Y., L.L.).

2Inquiries to Liping Li, Shantou University Medical College, Shantou,

eople’s Republic of China; e-mail: lpli@stu.edu.cn

© 2010 BY ELSEVIER INC. A002-9394/10/$36.00oi:10.1016/j.ajo.2009.08.015

VIDENCE FROM STUDIES IN CHINA,1–3 SINGAPORE,4

Hong Kong,5 Taiwan,6 and Australia7 suggests thatchildren of Chinese descent have among the world’s

ighest prevalence of myopia. Furthermore, this already-highrevalence of myopia among Chinese children8,9 and youngdults10 may be rising, though methodological questionsemain about some studies of this phenomenon.11

In order to explain the apparent rise in myopia preva-ence among children of Chinese ethnicity, a number ofotential environmental causative factors have been ex-mined. These have included increased near-work ac-ivity,12,13 higher levels of education,14 decreased outdoorctivity,15,16 and increasing population density.17

In China, improved nutrition in the two decades sincehe economic reforms of the early 1980s is believed to haveesulted in increases in height among recent cohorts whenompared to those born in previous years.18,19 It has beenheorized that a larger body habitus might be associatedith a greater axial length (AL) simply as a function of

arger overall body size.20 This relationship between in-reased height and longer AL has been reported amongingaporean Chinese schoolchildren21 and in a Singa-orean adult population.22

The association of height with refractive error (RE) isikely to be more complex than that with AL, because ofhe process of vision-driven emmetropization. In fact,tudies of height and RE have reported mixed results,ncluding the finding of greater stature among myopichildren,21 of no association,22,23 and of shorter heightsmong myopic individuals.24 Nonetheless, some authorsave proposed that nutritional differences might existetween myopic and nonmyopic individuals.25–27

We sought to examine the basic plausibility of the hypoth-sis that nutritional changes might underlie observed in-reases in the myopia prevalence among Chinese children.eight and weight among children during the teenage years,hen childhood myopia is most prevalent, may be assumed to

eflect a variety of factors, including the stage of puberty andenetic inheritance. In order to focus on those aspects oftature most directly responsive to nutritional intake, wehose to study stunting, which is defined with reference to atandard population assembled by the World Health Organi-ation (WHO)28 as height �2 standard deviations (SD)elow the mean for gender and age in months, that is, at the

.5th percentile or below. Stunting in children and teens is

LL RIGHTS RESERVED. 347

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enerally held to reflect poor nutritional intake over arolonged period of time.29 To the best of our knowledge,tunting has not previously been examined as an index ofutrition in myopic children.Our hypothesis is that, if improved nutrition could

lausibly explain recent increases in myopia prevalence,hen children identified on a cross-sectional basis with veryow height attributable to poor nutrition (stunting) oughto have significantly less myopia than children withormal or above-normal (overweight or obese) nutritionaltatus.

METHODS

HE “SEE WELL TO LEARN WELL” PROJECT IS AN ON-GOING

andomized trial of interventions to promote spectacleear among 10 000 secondary school children in 3 towns

n the rural Chaoshan region of Southern China. Partici-ants are selected at random from Year 1 and Year 2 classest all junior and senior high schools in the area.

SUBJECTS: All Year 1 and Year 2 classes (average sizepproximately 60 children) in all 5 junior high schools andhe 1 senior high school of Fuyang Township, Guangdongrovince, were enumerated and classes were selected atandom from a list of all eligible classes at each school untiltotal of 600 children (usually 8 to 10 classes) had been

dentified in the sampling frame. Our pilot testing in therea had demonstrated that participation rates were on

IGURE 1. Flow chart depicting the enrollment of rural Chin

he order of 80% to 85%, meaning that 600 children in the 2

AMERICAN JOURNAL OF48

ampling frame would be sufficient to guarantee a targetgure of 500 children examined at each school.Fuyang is located in the east of Guangdong province,

nd has a size of 38.5 square kilometers and a population of7 000 in 2004. It is located within 90 minutes’ drive ofhe city of Shantou (population 4.97 million at the endf 2006). The large majority of adults in Fuyang work inarming or agriculture.

MEASUREMENT OF VISUAL ACUITY AND REFRAC-

ION: Visual acuity (VA) with and without habitualefraction (if available) was measured by trained studyersonnel in well-lighted areas of the school during day-ight hours, at a distance of 5 meters, separately for eachye of each child. Children who did not have theirpectacles at school were asked to bring them for visionssessment on a separate day. Identical illuminated Snellenumbling E vision charts (Shantou City Medical Equip-ent Ltd, Shantou, China) were employed for all testing.he nontested eye was covered by the subject using aand-held occluder, with proper occlusion and neutralead position monitored by the examiner. The right eyeas tested first. A single optotype of each size was pre-

ented first, starting at 6/30. If a letter was failed, testingegan 2 lines above, with the child being asked to read allptotypes on the line sequentially. A subject had todentify correctly more than half of the letters on a givenine (eg, 3 out of 5, 4 out of 6) in order to be considered toave achieved that level of acuity.All subjects with vision of �6/12 in either eye, and a

choolchildren into a study of height, stunting, and myopia.

ese s

0% sample of children with vision �6/12 in both eyes,

OPHTHALMOLOGY FEBRUARY 2010

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nderwent cycloplegic autorefraction (Potec PRK-5000;otec Co Ltd, Seoul, Korea) with subjective refinementy an ophthalmologist in each eye, at least 30 minutesfter receiving cyclopentolate 1% (Cyclogyl; Alconaboratories, Fort Worth, Texas, USA) 1 drop to bothyes every 5 minutes, for a total of 2 drops in each eye.Figure 1) The results of subjective refraction aretilized throughout.

MEASUREMENT OF HEIGHT AND WEIGHT: Theeight in centimeters and weight in kilograms of allubjects were measured (RGZ-120 analog height measure-ent unit and scale, Jiangsu Suhong Medical Instrumentso Ltd, Changzhou, Jiangsu, People’s Republic of China)

nd recorded by trained study personnel (physicians), withhe children dressed in stocking feet and their usual schoollothing. The scale was zeroed at the beginning and end ofach morning’s and afternoon’s testing session. Height andeight were used to calculate the body mass index (BMI)f each subject according to the following formula: (weightn kg)/(height in m)2. The following terms were defined forubjects by gender and age in months with regard to anon-Chinese) standard WHO reference population:28

tunting (height �2 SDs below the mean of the referenceopulation for gender and age in months, ie, at the 2.5thercentile or below); overweight (�1 SD above the meanMI by age and gender); and obese (�2 SD above theean BMI by age and gender). The latter 2 definitions

TABLE 1. Demographic Characteristics, Vision, and Visual Fuon Refraction,

Data Complete

(n � 1371)

Age (years), mean (SD) 14.5 (1.4)

Gender, n (%)

Male 551 (40.2%)

Female 820 (59.8%)

Parents’ highest education, n (%)

Primary or below 266 (19.4%)

Junior school 708 (51.6%)

High school 272 (19.8%)

College or above 46 (3.4%)

Missing 79 (5.8%)

Uncorrected vision in the better eye, n (%)

�6/12 753 (54.9%)

�6/12 618 (45.1%)

Presenting vision in the better eye, n (%)

�6/12 388 (28.3%)

�6/12 983 (71.7%)

Refractive error in the better eye, mean (SD) �1.93 (1.82)

Visual function score, mean (SD) 76.1 (16.0)

SD � standard deviation; VA � visual acuity.aP value for the comparison between children with normal vision

pproach the standard adult cut-offs of BMI �25 kg/m2 m

STUNTING AND REFRACTIOL. 149, NO. 2

nd BMI �30 kg/m2 respectively as the age of the childpproaches 19 years.30

INTERVIEW DATA: All study subjects were adminis-ered a Chinese-language questionnaire prior to being toldhe results of their vision assessment. The basic question-aire included questions on age, gender, highest educa-ional attainment by either parent, child’s history of glassesear, and reasons for glasses nonwear. The questionnaire

ncluded a Chinese translation of an instrument developedriginally by Fletcher and associates, to assess self-reportedisual function (VF) in rural Asia.31 This instrument hasreviously been validated for use in Chinese subjects,32

nd is described elsewhere in detail.31

STATISTICAL METHODS: A two-tailed Student t testas applied for group comparison if the data wereormally distributed. For skewed data, the Mann–Whit-ey U test was used. The �2 test was employed toompare group differences for categorical variables. Theearson correlation was used to evaluate the associationetween spherical equivalent (SE) and height by gen-er. Moreover, multiple linear regression analysis waserformed to examine the association between SE andeight and nutritional indicators, adjusting for age andarental education and stratifying by gender. Quantita-ive data were summarized either in mean (SD) or

for 1371 Rural Chinese Schoolchildren With Complete Datat, and Weight

Normal Vision

(VA �6/12 Both Eyes)

(n � 355, 25.9%)

Low Vision

(Uncorrected VA �6/12 Either Eye)

(n � 1016, 74.1%) P valuea

14.1 (1.1) 14.6 (1.4) �.001

184 (51.8%) 367 (36.1%) �.001

171 (48.2%) 649 (63.9%)

68 (19.2%) 198 (19.5%) .707

179 (50.4%) 529 (52.1%)

77 (21.7%) 195 (19.2%)

10 (2.8%) 36 (3.5%)

21 (5.9%) 58 (5.7%)

0 (0.0%) 753 (74.1%) �.001

355 (100.0%) 263 (25.9%)

1 (0.3%) 387 (38.1%) �.001

354 (99.7%) 629 (61.9%)

�0.48 (0.82) �2.44 (1.80) �.001

86.1 (13.0) 72.8 (15.5) �.001

low vision.

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edian (interquartile range).

VE ERROR IN CHINA 349

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Statistical analyses were done using SPSS 14.0 (SPSS Inc,hicago, Illinois, USA). All statistical tests were two-sided,

nd a P value � .05 was considered statistically significant.

RESULTS

MONG 3,226 CHILDREN IN THE SAMPLE FRAME IN FUYANG

econdary schools, 2905 (90.0%) took part in the survey;mong those not taking part, 264 (8.2%) failed to obtainarental consent and 57 (1.8%) were absent from schooluring the survey period (Figure 1). Vision examinationsere completed on all but 0.2% of participants, while

efraction was carried out on a random 20% sample ofhildren with normal vision (n � 366) and 97% of those withncorrected VA �6/12 in either eye (n � 1,111). Amonghese 1477 children with refraction data, height and weightere measured for 1371 (92.8%) (Figure 1). These 1371hildren form the basis for the remaining analyses.

The mean age of children with complete data was4.5 � 1.4 years (range, 12 to 17 years), and 59.8% were girls.

TABLE 2. Analysis of Demographic Characteristics, Vision, Vi

Total Children

(n � 1364a)

Stunte

(n

Age (years), mean (SD) 14.5 (1.4) 14.7 (1.

Gender, n (%)

Male 549 (40.2%) 45 (51.7

Female 815 (59.8%) 42 (48.3

Height (cm), mean (SD) 155.7 (7.4) 144.4 (5.

BMI (kg/m2), median (interquartile

range) 18.0 (16.8 to 19.6) 17.0 (15

Parents’ highest education, n (%)

Primary or below 263 (19.3%) 23 (26.4

Junior school 705 (51.7%) 46 (52.9

High school 271 (19.9%) 11 (12.6

College or above 46 (3.4%) 4 (4.6%

Missing 79 (5.8%) 3 (3.4%

Presenting vision in the better eye,

n (%)

�6/12 386 (28.3%) 21 (24.1

�6/12 978 (71.7%) 66 (75.9

Child’s spherical equivalent in the

better, mean (SD) �1.93 (1.82) �1.91 (1

Visual function score, mean (SD) 76.1 (16.0) 76.9 (15

BMI � body mass index; SD � standard deviation.aOf the total 1371 subjects for whom height and weight m

overweight/obese were dropped from the analysis.bDefinition of stunting: height 2 SDs below the mean for age and gecDefinition of overweight: �1 SD above the mean BMI by age an

gender.dP value for the comparison between stunted children and overweP value for the comparison between stunted children and norma

he mean SE RE in the better-seeing eye was �1.93 � 1.82 g

AMERICAN JOURNAL OF50

iopters (D) (Table 1). Children with low vision (VA �6/12n either eye) were older, were significantly more likely to beirls, and had worse RE and self-reported visual function thanhildren with normal vision (Table 1).

The mean height and BMI for children with complete dataere 156 � 7 cm and 18.0 kg/m2 (interquartile range, 16.8 to9.6 kg/m2) (Table 2). Height and RE were inversely associ-ted (that is, taller children were more myopic) among boysr � �0.147; P � .001) but not girls (r � �0.046,; P � .193)Figure 2). Height and RE were not significantly associatedmong boys (P � .46) or girls (P � .85) when adjusting for age.

The RE and presenting vision of stunted children didot differ significantly from those of either normal orbese/overweight children (Table 2). The lack of signifi-ant difference between stunted and normal or obese/verweight children persisted when data were stratified byender (data not shown).

In multivariate models predicting SE-RE in the better-eeing eye, when adjusting for age and parental education,either stunting nor height was significantly associatedith RE for the group of children as a whole, or for boys or

unction, and Refractive Error According to Nutritional Status

renbOverweight/Obese

Childrenc

(n � 79)

Normal Children

(n � 1,198)

P

valuedP

valuee

14.0 (1.30) 14.5 (1.3) .002 .260

39 (49.4%) 465 (38.8%) .762 .017

40 (50.6%) 733 (61.2%)

158.0 (6.4) 156.4 (6.8) �.001 �.001

18.6) 24.1 (23.2 to 25.9) 18.0 (16.8 to 19.3) �.001 �.001

14 (17.7%) 226 (18.9%) .106 .170

44 (55.7%) 615 (51.3%)

15 (19.0%) 245 (20.5%)

0 (0.0%) 42 (3.5%)

6 (7.6%) 70 (5.8%)

20 (25.3%) 345 (28.8%) .860 .352

59 (74.7%) 853 (71.2%)

�1.72 (1.88) �1.94 (1.82) .506 .883

75.6 (13.7) 76.0 (16.2) .590 .659

ements were available, 7 children who are both stunted and

according to the World Health Organization reference population.28

der. Definition of obese: �2 SD above the mean BMI by age and

/obese children.

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The power of the study to have detected a difference of.50 D in RE between stunted and normal children was 0.77,hile the power to detect a difference of 0.75 D was 0.96.

DISCUSSION

ATA FROM THIS COHORT OF RURAL SECONDARY SCHOOL

hildren suggests that stunting is unassociated with RE for

IGURE 2. The association of height and spherical equivalentarticipating in a study of height, stunting, and myopia in rura

TABLE 3. Association Between Spherical Equivalent and HEducation and S

Independent Variables

All (n � 1285a)

� value Standard Error P value

Model no.1: Nutritional status

Not stuntedb NA NA NA

Stunted �0.030 0.200 .880

Model no. 2: Nutritional status

Stunted NA NA NA

Overweight/obesec 0.013 0.284 .965

Normal 0.031 0.201 .876

Model no. 3: Height

Height (cm) �0.004 0.008 .599

BMI � body mass index; NA � not applicable.aOf the total 1371 subjects for whom height and weight m

overweight/obese were dropped from the analysis, as were 79 subjebDefinition of stunting: height 2 standard deviation (SD) below th

reference population.28

cDefinition of overweight: �1 SD above the mean BMI by age and gen

ither girls or boys. We chose to examine the plausibility of c

STUNTING AND REFRACTIOL. 149, NO. 2

link between nutrition and RE by investigating aopulation with a high prevalence of both myopia andoor nutrition, while focusing on children among whomhe influence of nutrition on height is expected to be mostalient: children with stunting. Although some childrenre naturally of short stature attributable to their geneticndowment, when this prevalence exceeds 2.5% (2 SDselow the mean), as in this cohort where 87 of 13646.4%) subjects were stunted, it is expected that many

ctive error in the better eye for male and female schoolchildrenina.

and Nutritional Indicators, Adjusting for Age and Parentalying by Gender

Male (n � 513a) Female (n � 772a)

alue Standard Error P value � value Standard Error P value

A NA NA NA NA NA

.191 0.263 .469 0.154 0.298 .605

A NA NA NA NA NA

.170 0.375 .651 �0.165 0.422 .697

.193 0.265 .467 �0.154 0.298 .607

.006 0.010 .531 �0.0004 0.014 .974

ements were available, 7 children who are both stunted and

ale � 36, female � 43) missing data for parents’ highest education.

n for age and gender according to the World Health Organization

efinition of obese: �2 SD above the mean BMI by age and gender.

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ur failure to detect a difference in myopia prevalenceetween stunted children and those with normal stature,r children with overweight/obesity (thus eliminatingubjects with borderline nutritional status), is not consis-ent with a causative role for nutrition in the developmentf myopia in this population. This lack of an associationersisted when adjusting for age and parental educationnd stratifying by gender.

We considered the possibility that children of Chineseescent might naturally be of shorter stature than thehildren making up the WHO reference population. How-ver, when similar standard populations have been used toeasure ethnically Chinese children in economically less

isadvantaged areas, the prevalence of stunting has beenery low (for example, 0.2% in Singapore in 2000).33

hus, it would appear unlikely that a large proportion ofhe ethnically Chinese children classified as stunted ac-ording to the current study are in fact of shorter statureolely for genetic reasons.

Given the large number of children included in ourample and the relatively high prevalence of RE and poorutrition, the power to have detected visually significantifferences in RE between stunted and normal childrenas adequate.The results of this study must be understood within the

ontext of its limitations. Though a high prevalence oftunting as observed in this setting provides strong evi-ence of nutritional insufficiency among affected individ-als, we did not attempt to validate this with otherutritional indicators such as dietary recall or a record ofctual calories consumed. Height and weight measures asssessed by WHO cut-offs against the WHO standardopulation have been validated as robust indicators of

utritional status.34 y

2888–2894.

AMERICAN JOURNAL OF52

Secondly, our study was cross-sectional, which meanthat the hypothesis that change in myopia status over times linked to longitudinal variations in nutriture could note directly examined. However, for this hypothesis to bealid, a minimum condition is that myopia and nutritionaltatus should be causally linked. Our cross-sectional datan stunting and myopia are not consistent with suchinkage.

Our sampling strategy over-sampled for children withyopia. Thus, it is possible that we failed to detect an

ssociation between myopia and stunting because of thearge number of myopic children included relative to thoseithout myopia. In order to reduce the chances of this,owever, we did include a 20% random sample of childrenith normal (�6/12) uncorrected vision in both eyes, andltimately obtained complete data on 355 such subjects,ome 26% of our total cohort.

Finally, our study design did not include an exhaustiveurvey of all potential environmental associations withyopia, potentially including near work,12,13 outdoor ac-

ivity,15,16 and population density.17 The possibility muste considered that an association might have been ob-erved between stunting and RE if these potential con-ounding factors had been measured and adjusted for.resumably, a strong association between stunting and REould have been detected with the current study design.Despite its limitations, this is one of the first studies to

irectly examine the association between stunting and REn a population at high-risk for both RE and poor nutri-ion. Our results do not appear consistent with a strongausative role for nutrition in determining the observedhanges in RE occurring among Chinese children in recent

ears.

HIS STUDY WAS SUPPORTED BY A GRANT TO OXFORD UNIVERSITY FROM THE LI KA SHING FOUNDATION, HONG KONG,hina (the See Well to Learn Well Project). The authors indicate no financial conflict of interest. Involved in design and conduct of study (N.C., Y.G.,.S.C.L., L.L., M.Z., Y.S., S.G.); collection, management, analysis, and interpretation of data (A.S., N.C., Y.G., Y.L., Y.Y., Jin.W., Jia.W., Y.K.T.); andreparation, review, or approval of the manuscript (N.C., Y.G., Y.L., Y.Y., Jin.W., D.S.C.L., L.L., Jia.W., Y.K.T., M.Z., Y.S., S.G.). The protocol haseen approved in full by the Ethics Committees at the Chinese University of Hong Kong and the Joint Shantou International Eye Center, Guangdongrovince, China, and by the tenets of the Declaration of Helsinki.

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Biosketch

bhishek Sharma, MBBS, is a medical doctor from Australia, graduating from University of Tasmania in 2004, andompleted a Masters in Medicine from University of Sydney in 2008. He is currently completing a DPhil in Public Healthrom the University of Oxford as a Rhodes Scholar, working on the Xichang Pediatric Refractive Error Study inonjunction with Chinese University of Hong Kong. He is interested in clinical science and public health research inyopia.

AMERICAN JOURNAL OF OPHTHALMOLOGY53.e1 FEBRUARY 2010