February 2014
Volume 55, Issue 2
Free
Physiology and Pharmacology  |   February 2014
Parapapillary Beta Zone in Primary School Children in Beijing: Associations With Outdoor Activity
Author Affiliations & Notes
  • Yin Guo
    Tongren Eye Care Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China
  • Li Juan Liu
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China
  • Liang Xu
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China
  • Yan Yun Lv
    Tongren Eye Care Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China
  • Ping Tang
    Tongren Eye Care Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China
  • Yi Feng
    Tongren Eye Care Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China
  • Jin Qiong Zhou
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China
  • Meng Meng
    Tongren Eye Care Center, Beijing Tongren Hospital, Capital Medical University, Beijing, China
  • Jost B. Jonas
    Beijing Institute of Ophthalmology, Beijing Tongren Hospital, Capital Medical University, Beijing, China
    Department of Ophthalmology, Medical Faculty Mannheim of the Ruprecht-Karls-University Heidelberg, Heidelberg, Germany
  • Correspondence: Liang Xu, Beijing Institute of Ophthalmology, 17 Hougou Lane, Chong Wen Men, 100005 Beijing, China; xlbio1@163.com
  • Jost B. Jonas, Universitäts-Augenklinik, Kutzerufer 1, 68167 Mannheim, Germany; Jost.Jonas@medma.uni-heidelberg.de
Investigative Ophthalmology & Visual Science February 2014, Vol.55, 918-925. doi:10.1167/iovs.13-13502
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      Yin Guo, Li Juan Liu, Liang Xu, Yan Yun Lv, Ping Tang, Yi Feng, Jin Qiong Zhou, Meng Meng, Jost B. Jonas; Parapapillary Beta Zone in Primary School Children in Beijing: Associations With Outdoor Activity. Invest. Ophthalmol. Vis. Sci. 2014;55(2):918-925. doi: 10.1167/iovs.13-13502.

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      © ARVO (1962-2015); The Authors (2016-present)

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Abstract

Purpose.: To investigate prevalence and size of parapapillary alpha zone and beta zone and associations with myopia-related factors in primary school children in Beijing.

Methods.: The school-based study included 382 grade-1 children and 299 grade-4 children. The children underwent a comprehensive eye examination and the parents, an interview. The examination was repeated after 1 year.

Results.: Beta zone (prevalence: 44.5% ± 2.1%; mean area: 0.17 ± 0.29 mm2) was significantly associated with more time spent indoors with studying (P = 0.004; standardized correlation coefficient β: 0.14; regression coefficient B: 0.05; 95% confidence interval [CI]: 0.02, 0.09) after adjusting for longer axial length (P < 0.001; β: 0.22; B: 0.07; 95% CI: 0.04, 0.10), more myopic refractive error (P < 0.001; β: −0.29; B: −0.07; 95% CI: −0.09, −0.04), region of habitation (P = 0.03; β: 0.11; B: 0.07; 95% CI: 0.01, 0.14), and vertical disc diameter (P = 0.03; β: 0.10; B: 0.16; 95% CI: 0.02, 0.30). As a corollary, indoors studying time was associated with larger area of beta zone (P = 0.01; β: 0.11; B: 0.30; 95% CI: 0.07, 0.54) after adjusting for higher axial length/corneal curvature radius ratio (AL/CC; P = 0.006; β: 0.12; B: 0.94; 95% CI: 0.27, 1.62) and urban region of habitation (P < 0.001; β: −0.44; B: −0.75; 95% CI: −0.89, −0.61). An increase in AL/CC ratio at 1-year follow-up was associated with more indoors studying time (P = 0.04; β: 0.10; B: 0.01; 95% CI: 0.00, 0.01) and larger beta zone area (P < 0.001; β: 0.19; B: 0.04; 95% CI: 0.02, 0.05) after adjusting for axial length (P < 0.001; β: −0.21; B: −0.01; 95% CI: −0.02, −0.01).

Conclusions.: Larger parapapillary beta zone area was associated with more indoors studying time after adjustment for axial length, refractive error, and region of habitation, and reversely, more indoors studying time was associated with larger beta zone in multivariate analysis. The results could indicate that parapapillary beta zone is associated with external factors–dependent development of myopia.

Introduction
Recent histologic, clinical, and epidemiologic studies have shown that the parapapillary region can be differentiated into several zones. 18 Upon ophthalmoscopy, the peripheral alpha zone is characterized by irregular pigmentation. It corresponds histologically and in optical coherence tomograms (OCTs) with an irregularly structured retinal pigment epithelium resting on an intact Bruch's membrane. Beta zone, located between alpha zone and the optic disc border, shows visible large choroidal vessels and visible sclera on fundus photographs. Histologically and on OCT images, this ophthalmoscopic beta zone could further be subdivided into a region in which Bruch's membrane is present but denuded from retinal pigment epithelium (“histologic beta zone”), and into a central region at the optic disc border in which Bruch's membrane is not present. 3,5 This latter region has been called “gamma zone.” Prevalence and size of alpha and beta zone, as measured on fundus photographs, has been determined in many previous studies that also revealed an association of the ophthalmoscopic beta zone with presence, severity, and progression of glaucomatous optic neuropathy or with myopia. 1,2,7 If in histologic studies and clinical OCT-based investigations the ophthalmoscopic beta zone is split up into histologic beta zone and gamma zone, the histologic beta zone is associated with glaucoma but not with axial myopia, while gamma zone is associated with axial myopia, however not with glaucoma. 3,5 Since by ophthalmoscopy or on fundus photographs one cannot clearly distinguish between the histologic beta zone and gamma zone, both zones have up to now been summarized as ophthalmoscopic beta zone in clinical practice. Although many previous studies have focused on the parapapillary zones, only few investigations have addressed the prevalence, size, and associations of the parapapillary zones in eyes of children. 913 Parapapillary zones may however be of interest in children, in particular in China, since the ophthalmoscopic beta zone is associated with axial myopia, and China as other countries in East and Southeast Asia has witnessed a marked increase in the prevalence and severity of axial myopia in the young generation. 14 We therefore measured the parapapillary zones in a sample of school children from Beijing. We included different school grades and also assessed the outdoor/indoor activity and other myopia-related factors to assess in a multivariate analysis which parameters besides axial myopia were associated with the parapapillary regions. 
Methods
The study included children attending primary schools (grade 1 and grade 4) from rural regions and urban areas of Greater Beijing. 15 The Human Research Medical Ethics Committee of the Beijing Tongren Hospital approved the study protocol and all participants gave informed consent, according to the Declaration of Helsinki. After explanation of the study design to parents and children, informed written consent was obtained from at least one parent per child. 
As study sites we chose two regions, the Beijing Dong Cheng district and the Beijing Huai Rou district, with marked differences in mean income and socioeconomic background. The urban Dong Cheng district was located in the center of Beijing city. The average income was 30,684 yuan in 2010, which was considerably higher than the average income across the whole of Beijing (19,640 yuan). The rural Huai Rou district was located in the southeast of Beijing at a distance of 40 kilometers from the center of Beijing. The average income was 11,012 yuan. 
The children underwent a comprehensive eye examination including measurement of visual acuity and autorefractometry, assessment of ocular motility, slit lamp–assisted biomicroscopy of the anterior and posterior segment of the eye, and nonmydriatic digital fundus photography (45°, CR-DGI camera; Canon Inc., Tokyo, Japan). Ocular biometric parameters (central corneal thickness, corneal curvature, anterior chamber depth, lens thickness, axial length) were measured for the right eye of all subjects by optical low-coherence reflectometry (Lensstar 900 Optical Biometer; Haag-Streit, Koeniz, Switzerland). We additionally calculated the ratio of axial length to anterior corneal curvature as surrogate for refractive error. Refractometry was performed in a noncycloplegic state by autorefractometry (auto-refractor KR-8900; Topcon, Tokyo, Japan) followed by subjective refractometry. The spherical equivalent of the refractive error was calculated as spherical refractive error + ½ cylindrical refractive error. All examinations were carried out by trained ophthalmologists and optometrists. We additionally calculated the ratio of axial length divided by anterior corneal curvature (AL/CC), which has also been known as the AL/CR (axial length/corneal radius) ratio and which has been used as surrogate for refractive error. Since it includes corneal refractive power, it is a better correlate for refractive error than is axial length as a single parameter. 16  
The parents underwent an interview. The questionnaire included questions about how long the children needed to go to school and to return home; what kind of transportation (walking, bicycle, private car, public transport) was taken; how long the children spent outdoors during school breaks; what kind of sport the children played and how long they performed it during the week and during the weekends. The assessment of the time spent outdoors was based on questions about walking, playing outdoors, having picnics, and playing outdoor sports. The total outdoor activity was defined as the sum of outdoor leisure and outdoor sports. The interview additionally included questions about the time used to study indoors, about the time of watching television, and the time to play with electronic devices indoors. The average time spent daily on these activities was calculated by using the formula [(hours spent on a weekday) × 5 + (hours spent on a weekend day) × 2]/7. We additionally asked about the birth weight, mother's age at birth, being breast-fed, smoking and alcohol consumption of father and mother, level of education and profession of the parents, size of the house (in m2), monthly family income, and prevalence of myopia of the parents. 
Parapapillary regions were identified and measured on the fundus photographs. Alpha zone was characterized by an irregular hypopigmentation and hyperpigmentation, and intimated thinning of the chorioretinal tissue layer. On its outer side it was adjacent to the retina, and on its inner side it was in touch with the beta zone, or if the beta zone was not present, with the peripapillary ring of the optic disc margin. Features of the beta zone included good visibility of the large choroidal vessels and the sclera, thinning of the chorioretinal tissues, and round bounds to the adjacent alpha zone on its peripheral side and to the peripapillary ring on its central side. The outlines of the alpha zone and beta zone were plotted by using a mouse-driven cursor to trace the margins directly onto the image with Image J software (version 1.43u; developed by Wayne Rasband, National Institutes of Health, Bethesda, MD; available in the public domain at http://rsb.info.nih.gov/ij/index.html). The pixel area of the structure measured was then determined. The magnification of ImageJ was ×175. Combined with the magnification factor of ×1.4 by the fundus camera, the total magnification by the camera and ImageJ system was ×245. We then corrected for the magnification by the optic media of the eye, applying the method of Littmann, 17 using either the axial length measurements or the refractive error measurements. In addition to the parapapillary zones, the area and diameters of the optic disc and cup were measured. The measurements were performed by a trained ophthalmologist (YG) supervised by a panel of glaucoma specialists (LX, JBJ). During the period of measurement of the parapapillary region, the panel convened several times to discuss and decide upon questionable cases. In addition, cases were randomly selected and checked for accuracy of the measurements. 
One year after the baseline examination, the children were re-examined using the same techniques. 
Inclusion criterion for the present study was the availability of fundus photographs of sufficient quality to assess the parapapillary zones. Statistical analysis was performed by using a commercially available statistical software package (SPSS for Windows, version 21.0; SPSS, Chicago, IL). The parameters were presented as mean ± SD. The normal distribution of the parameters was examined by applying the Kolmogorov-Smirnoff test. To examine the associations between parapapillary regions and other parameters, such as refractive error, socioeconomic parameters, and outdoor activity, the χ2 test was applied for categorical variables and a logistic regression analysis for continuous variables. After univariate analysis of potential associations, we performed a stepwise multivariate analysis with presence of the parapapillary region as dependent variable, and as independent variables, all parameters that showed a significant association with the main parameters in univariate analysis. For the area and width of parapapillary region, we applied a multivariate linear regression analysis with the area or width parameter as dependent variable, and as independent variables, all those parameters that were significantly associated with the area or width parameter in the univariate analysis. Odds ratios were calculated and 95% confidence intervals (CI) were presented. All P values were two sided and were considered statistically significant when the values were less than 0.05. 
Results
Of 690 eligible students in both schools, 681 (98.7%) children participated in the study. At the examination day, 7 children were at home because of illness and 2 children did not participate in the investigation for no obvious reason. The whole study population was divided into 382 (56.1%) students from grade 1 with a mean age of 6.3 ± 0.5 years (range, 5–8 years) and into 299 (43.9%) students from grade 4 with a mean age of 9.4 ± 0.7 years (range, 8–13 years). Of the 681 children, 370 (54.3%) students were living in the urban region. The mean refractive error of the worse eye was −0.62 ± 1.42 diopters (D; median: −0.50 D; range, −7.38 to +7.25 D). Mean axial length was 23.03 ± 0.96 mm (median: 22.99 mm; range, 19.01–26.17 mm) and the mean AL/CC ratio was 2.94 ± 0.11. 15  
Among these 681 children, fundus photographs of sufficient quality to assess the parapapillary regions were available for 562 (82.5%) children. The children with fundus-accessible photographs, compared with the children without those photographs, were significantly older (7.8 ± 1.7 years vs. 7.1 ± 1.6 years; P < 0.001), had a significantly longer axial length (23.1 ± 1.0 mm vs. 22.8 ± 0.9 mm; P = 0.005), had a higher AL/CC ratio (2.95 ± 0.11 vs. 2.91 ± 0.09; P < 0.001), and were more myopic (−0.64 ± 1.26 D vs. −0.01 ± 1.41 D; P < 0.001). 
Alpha zone was found in 531 subjects (531/562; prevalence: 94.5% ± 1.0% [95% CI: 92.6, 96.4]). It occurred significantly (P < 0.001) more often in the temporal peripapillary region (530/562; 94.3%) than in the inferior region (123/562; 21.9%), the superior region (187/562; 33.3%), and the nasal region (2/562; 0.4%). Mean area of alpha zone measured 0.36 ± 0.16 mm2 (median: 0.36 mm2; range, 0.00–1.15 mm2). Mean widest alpha zone was 0.25 ± 0.09 mm (median: 0.26 mm; range, 0.00–0.62 mm). The region of greatest alpha zone was temporal in 529 (94.1%) eyes. 
In univariate analysis, the area of alpha zone was significantly associated with older age (P = 0.04; correlation coefficient r: 0.09), taller body height (P = 0.04; r: 0.09), longer axial length (P = 0.04; r: 0.09), higher AL/CC ratio (P < 0.001; r: 0.15), more myopic refractive error (P < 0.001; r: −0.22), myopia of mother (P = 0.01), less outdoor activity (P = 0.003; r: −0.15), and larger size (P = 0.02) of beta zone. It was not significantly associated with school grade (P = 0.06), myopia of the father (P = 0.21), indoor time spent with studying (P = 0.21), and indoor time spent with watching television (P = 0.35). 
In multivariate analysis, area of alpha zone was significantly associated with a larger beta zone (P = 0.02; standardized correlation coefficient β: 0.14; regression coefficient B: 0.07; 95% CI: 0.02, 0.13), and it was marginally associated with higher AL/CC ratio (P = 0.06; β: 0.11; B: 0.16; 95% CI: −0.01, 0.33) and less time spent outdoors (P = 0.07; β: −0.10; B: −0.02; 95% CI: −0.05, 0.00). If size of beta zone was dropped and age was added, area of alpha zone was significantly associated with less time spent outdoors (P = 0.04; β: −0.12; B: −0.03; 95% CI: −0.05, 0.00). 
Beta zone was found in 250 subjects (250/562; prevalence: 44.5% ± 2.1% [95% CI: 40.4, 48.6]). It occurred significantly (P < 0.001) more often in the temporal peripapillary region (244/562; 43.4%) than in the inferior region (124/562; 22.1%), the superior region (113/562; 20.1%), and the nasal region (10/562; 1.8%). Mean area of beta zone measured 0.17 ± 0.29 mm2 (median: 0.00 mm2; range, 0.00–2.65 mm2). Mean widest beta zone was 0.11 ± 0.15 mm (median: 0.00 mm; range, 0.00–1.08 mm). The region of greatest beta zone was temporal in 214 eyes (85.6%), followed by inferior in 27 (10.8%) eyes, superior in 6 (2.4%) eyes, and nasal in 3 (1.2%) eyes. Applying the Kolmogorov-Smirnoff test revealed that beta zone area was not normally distributed (P < 0.001). We therefore took the logarithm of beta zone area (which was normally distributed [P = 0.95]) for further regression analysis. 
In univariate analysis, area of beta zone was significantly associated with older age, female sex, maternal myopia, white collar occupation by mother and father, taller body height, urban region of habitation, higher school grade, less time outdoors, more time indoors spent with studying (Figure), longer axial length, deeper anterior chamber, more myopic refractive error, and shorter horizontal optic disc diameter (Tables 1, 2). 
Figure
 
Scattergram showing the association between the time spent indoors with studying and the area of parapapillary beta zone.
Figure
 
Scattergram showing the association between the time spent indoors with studying and the area of parapapillary beta zone.
Table 1.
 
Associations (Univariate Analysis) Between the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Table 1.
 
Associations (Univariate Analysis) Between the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Age, y <0.001 0.21 0.04 0.02, 0.05
Sex 0.37
Maternal myopia 0.009 0.12 0.08 0.02, 0.13
Paternal myopia 0.32
Birth weight, kg 0.68
Maternal age at birth, y 0.32
Mother's occupation (blue collar/white collar) 0.08 0.09 0.06 −0.01, 0.12
Father's occupation (blue collar/white collar) 0.009 0.12 0.07 0.02, 0.13
Smoking by mother 0.58
Smoking by father 0.62
Body height, cm <0.001 0.20 0.005 0.003, 0.008
Body weight, kg 0.25
Body mass index, kg/m2 0.31
Urban/rural region of habitation 0.08 −0.08 −0.05 −0.09, 0.01
School grade <0.001 0.25 0.05 0.03, 0.07
Time spent outdoors 0.03 −0.12 −0.05 −0.09, −0.01
Time spent indoors studying <0.001 0.19 0.07 0.04, 0.10
Axial length, mm <0.001 0.33 0.10 0.08, 0.12
Corneal curvature radius, mm 0.31
Anterior chamber depth, mm <0.001 0.21 0.23 0.14, 0.32
Axial length/corneal curvature radius <0.001 0.33 0.88 0.67, 1.09
Refractive error, D <0.001 −0.35 −0.08 −0.10, −0.06
Best-corrected visual acuity 0.24
Horizontal optic disc diameter 0.04 −0.09 −0.14 −0.27, −0.01
Vertical optic disc diameter 0.46
Horizontal optic cup diameter 0.87
Vertical optic cup diameter 0.87
Table 2.
 
Associations (Univariate Analysis) Between the Logarithm of the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Table 2.
 
Associations (Univariate Analysis) Between the Logarithm of the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Age, y <0.001 0.27 0.05 0.03, 0.08
Sex 0.04 0.13 0.09 0.001, 0.17
Maternal myopia 0.005 0.18 0.13 0.04, 0.22
Paternal myopia 0.32
Birth weight, kg 0.94
Maternal age at birth, y 0.16
Mother's occupation (blue collar/white collar) 0.01 0.18 0.13 0.03, 0.23
Father's occupation (blue collar/white collar) 0.02 0.17 0.11 0.02, 0.21
Smoking by mother 0.81
Smoking by father 0.99
Body height, cm <0.001 0.34 0.010 0.006, 0.013
Body weight, kg 0.02 0.17 0.007 0.001, 0.013
Body mass index, kg/m2 0.17
Urban/rural region of habitation 0.03 −0.14 −0.10 −0.18, −0.01
School grade <0.001 0.31 0.07 0.04, 0.10
Time spent outdoors <0.001 −0.128 −0.12 −0.18, −0.05
Time spent indoors studying 0.001 0.24 0.10 0.104, 0.15
Axial length, mm <0.001 0.29 0.09 0.05, 0.13
Corneal curvature radius, mm 0.55
Anterior chamber depth, mm <0.001 0.23 0.27 0.13, 0.40
Axial length/corneal curvature radius <0.001 0.36 0.95 0.63, 1.26
Refractive error, D <0.001 −0.33 −0.08 −0.10, −0.05
Best-corrected visual acuity 0.99
Horizontal optic disc diameter 0.04 −0.13 −0.20 −0.40, −0.01
Vertical optic disc diameter 0.62
Horizontal optic cup diameter 0.05 −0.12 −0.18 −0.36, 0.00
Vertical optic cup diameter 0.13
The multivariate regression analysis included beta zone area as dependent variable and all those parameters as independent variables that were (here defined as P < 0.10) associated with beta zone area in the univariate analysis. We then dropped step by step school grade (variance inflation factor: 9.8), father's occupation (variance inflation factor: 3.4), AL/CC ratio (variance inflation factor: 3.3), mother's occupation (P = 0.84), anterior chamber depth (P = 0.47), time spent outdoors (P = 0.57), body height (P = 0.23), maternal myopia (P = 0.17), and horizontal disc diameter (P = 0.07). In the final model, the area of beta zone remained significantly (correlation coefficient r: 0.45) associated with more time spent indoors with studying (P = 0.004), after adjusting for longer axial length (P < 0.001), more myopic refractive error (P < 0.001), longer vertical optic disc diameter (P = 0.03), and region of habitation (P = 0.03; Table 3). 
Table 3.
 
Associations (Multivariate Analysis) Between the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters*
Table 3.
 
Associations (Multivariate Analysis) Between the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters*
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Time spent indoors 0.004 0.14 0.05 0.02, 0.09
Axial length, mm <0.001 0.22 0.07 0.04, 0.10
Refractive error (spherical equivalent), D <0.001 −0.29 −0.07 −0.09, −0.04
Vertical optic disc diameter 0.03 0.10 0.16 0.02 , 0.30
Urban/rural region of habitation 0.03 0.11 0.07 0.01, 0.14
In a similar manner, the logarithm of parapapillary beta zone area was significantly (correlation coefficient r: 0.43) associated with time spent indoors with studying (P = 0.04), longer axial length (P = 0.007), more myopic refractive error (P = 0.007), and longer vertical optic disc diameter (P = 0.02; Table 4). If the parameters of axial length and refractive error were replaced by the AL/CC ratio, the logarithm of parapapillary beta zone area was significantly (correlation coefficient r: 0.44) associated with the time spent indoors with studying (P = 0.03), higher AL/CC ratio with longer axial length (P < 0.001), and longer vertical optic disc diameter (P = 0.003) 
Table 4.
 
Associations (Multivariate Analysis) Between the Logarithm of the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Table 4.
 
Associations (Multivariate Analysis) Between the Logarithm of the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Time spent indoors 0.04 0.14 0.06 0.00, 0.12
Axial length, mm 0.007 0.21 0.06 0.02, 0.11
Refractive error (spherical equivalent), D 0.007 −0.21 −0.05 −0.08, −0.01
Vertical optic disc diameter 0.02 0.16 0.27 0.04, 0.51
Time spent indoors with studying was significantly associated (univariate analysis) with maternal and paternal myopia, white collar occupation of mother and father, taller body height, urban region of habitation, higher school grade, less time spent outdoors, longer axial length, deeper anterior chamber, higher AL/CC ratio, more myopic refractive error, longer vertical optic disc and cup diameter, and larger area of beta zone (Table 5). In the multivariate analysis, we first dropped vertical optic cup diameter (variance inflation factor: 10.9), father's occupation (variance inflation factor: 3.5), smoking by the mother (P = 0.65), time spent outdoors (P = 0.70), mother's occupation (P = 0.47), paternal myopia (P = 0.71), maternal myopia (P = 0.83), anterior chamber depth (P = 0.59), horizontal optic cup diameter (P = 0.37), axial length (P = 0.66), refractive error (P = 0.23), body height (P = 0.14), and vertical disc diameter (P = 0.68). In the final model, time spent indoors with studying was significantly (regression coefficient: r = 0.52) associated with larger area of beta zone (P = 0.01), higher AL/CC ratio (P = 0.006), and urban region of habitation (P < 0.001; Table 6
Table 5.
 
Associations (Univariate Analysis) Between the Time Spent Indoors With Studying and Ocular and Systemic Parameters
Table 5.
 
Associations (Univariate Analysis) Between the Time Spent Indoors With Studying and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Age, y 0.12
Sex 0.52
Maternal myopia 0.002 0.15 0.26 0.10, 0.43
Paternal myopia 0.04 0.10 0.19 0.01, 0.36
Birth weight, kg 0.39
Maternal age at birth, y 0.12
Mother's occupation (blue collar/white collar) <0.001 0.32 0.54 0.37, 0.70
Father's occupation (blue collar/white collar) <0.001 0.42 0.70 0.56, 0.85
Smoking by mother 0.07 −0.09 −0.33 −0.69, −0.03
Smoking by father 0.15
Body height, cm 0.03 0.11 0.008 0.001, 0.02
Body weight, kg 0.24
Body mass index, kg/m2 0.91
Urban/rural region of habitation <0.001 −0.48 −0.81 −0.95, −0.67
School grade 0.04 0.10 0.05 0.002, 0.11
Time spent outdoors <0.001 −0.35 −0.41 −0.53, −0.30
Axial length, mm <0.001 0.18 0.15 0.07, 0.23
Corneal curvature radius, mm 0.26
Anterior chamber depth, mm 0.006 0.13 0.40 0.12, 0.69
Axial length/corneal curvature radius <0.001 0.25 1.92 1.23, 2.62
Refractive error, D <0.001 −0.25 −0.16 −0.22, −0.11
Best-corrected visual acuity 0.50
Horizontal optic disc diameter 0.32
Vertical optic disc diameter 0.003 −0.14 −0.62 −1.04, −0.21
Horizontal optic cup diameter 0.06 −0.09 −0.33 −0.68, 0.01
Vertical optic cup diameter 0.02 −0.12 −0.40 −0.73, −0.08
Beta zone area, mm2 <0.001 0.19 0.50 0.26, 0.75
Table 6.
 
Associations (Multivariate Analysis) Between the Time Spent Indoors With Studying and Ocular and Systemic Parameters
Table 6.
 
Associations (Multivariate Analysis) Between the Time Spent Indoors With Studying and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Parapapillary beta zone area, mm2 0.01 0.11 0.30 0.07, 0.54
Urban/rural region of habitation <0.001 −0.44 −0.75 −0.89, −0.61
Axial length/corneal curvature radius ratio 0.006 0.12 0.94 0.27, 1.62
Of the 681 students examined at baseline in 2011, 643 (94.4%) returned for the follow-up examination in 2012. As reported recently, the mean refractive error changed by −0.06 ± 0.89 D, mean axial length elongated by 0.26 ± 0.49 mm, and the mean AL/CC ratio increased by 0.03 ± 0.06. The mean time spent daily outdoors (2.0 ± 0.8 hours) increased by 0.4 ± 0.9 hours, and the mean time spent daily indoors with studying (5.5 ± 0.9 hours) increased by 0.2 ± 1.0 hours. In multivariate analysis, an increase in AL/CC was significantly associated with more indoors studying time (P = 0.04; β: 0.10; B: 0.01; 95% CI: 0.00, 0.01) and larger beta zone area (P < 0.001; β: 0.19; B: 0.04; 95% CI: 0.02, 0.05) after adjusting for axial length (P < 0.001; β: −0.21; B: −0.01; 95% CI: −0.02, −0.01). Of the whole study population, 570 (88.6%) children showed an increase in axial length. An increase in axial length was associated with more indoors studying time (P = 0.009; β: 0.13; B: 0.08; 95% CI: 0.02, 0.14) and larger beta zone area (P < 0.001; β: 0.19; B: 0.30; 95% CI: 0.14, 0.46) after adjusting for axial length (P < 0.001; β: −0.27; B: −0.14; 95% CI: −0.19, −0.09). Correspondingly, larger beta zone at baseline was associated with a greater change in the AL/CC ratio (P < 0.001; β: 0.17; B: 0.91; 95% CI: 0.42, 1.41) after adjusting for more time spent indoors with studying (P = 0.03; β: 0.11; B: 0.04; 95% CI: 0.01, 0.08) and longer axial length (P < 0.001; β: 0.34; B: 0.11; 95% CI: 0.08, 0.14). 
Discussion
In our school-based study, larger parapapillary beta zone area was associated with more indoors studying time after adjustment for axial length, refractive error, and region of habitation. As a corollary, more indoors studying time was significantly associated with a larger area of beta zone after adjusting for a higher AL/CC ratio and urban region of habitation. In the follow-up examination, an increase in the AL/CC ratio and in axial length was significantly associated with more indoors studying time and larger beta zone area. 
The prevalence of beta zone as detected in our study population was higher than in previous studies on children or adults. In the Sydney Childhood Eye Study, 1765 children aged 6 years were examined and OCT optic-disc measurements were taken. 12 The prevalence of beta zone is reported at 20.2%. In the Beijing Eye Study on adult Chinese aged 40 years or older, prevalence of beta zone is 19.9%. 18 The difference between the studies on the prevalence of beta zone may be explained by the difference in the prevalence of myopia, with children in China now being more often and more severely myopic than children in Sydney or than adults in Beijing. 19 In all studies, beta zone was most prevalent and widest in the temporal parapapillary region, and least frequent and smallest in the nasal region, and in most previous studies as in the present investigation, beta zone was associated with axial length or myopic refractive error. To cite an example, in the study by Tong and colleagues 9 on children from Singapore, a myopic temporal crescent is associated only with a longer axial length. The parapapillary atrophy to optic disc area ratio is much greater in the subjects with myopia than those with emmetropia. As a corollary, myopia severity is associated with increased parapapillary atrophy and oval shape of the disc. In multiple regression, increased parapapillary atrophy to optic disc area ratio is associated with increased axial length, increased myopia severity, and increasing age. 9  
In our study, the area of beta zone was significantly associated with more indoors studying time after adjusting for longer axial length, more myopic refractive error, and rural region of habitation. Correspondingly, the indoors studying time was significantly associated with a larger area of beta zone after adjusting for a higher AL/CC ratio and urban region of habitation. Previous studies, as well as the present investigation, have shown an association between less time spent on outdoor activities or more indoors time and the prevalence and amount of myopia. 2025 The question arises whether the association between more indoors time (or less outdoors time) and larger beta zone could indicate that parapapillary beta zone is associated with external factors–dependent development of myopia. Previous studies have shown that the prevalence of myopia and axial length is associated with fixed parameters, such as the genetic pattern, 26,27 and modifiable parameters such as indoors/outdoors activities. 2025 If further studies confirm an association of parapapillary beta zone with indoors/outdoors activity after adjusting for axial myopia, it could suggest that external factors, such as indoors/outdoors activities, influence the development of myopia in association with parapapillary beta zone. Fitting with that hypothesis, prevalence and size of beta zone were not related with parental myopia in our study population. If there is an association between parapapillary beta zone and indoors/outdoors activity, the amount of beta zone may potentially be a surrogate for the amount of myopia modifiable by a change in lifestyle. Correspondingly, an increase in the AL/CC ratio and in axial length during the 1-year follow-up was significantly associated with more indoors studying time and with larger beta zone area. 
Interestingly, the prevalence of beta zone in our young study population (prevalence: 44.5% ± 2.1% [95% CI: 40.4, 48.6]) was markedly higher than in the population of the Beijing Eye Study (beta zone prevalence: 19.9% ± 0.6% [95% CI: 18.7, 21.2]) with a mean age of 64.6 ± 9.8 years (range, 50–93 years). These populations did not markedly differ in refractive error (−0.62 ± 1.42 D [range, −7.38 to +7.25 D; noncycloplegic] vs. −0.20 ± 2.07 D [median: +0.20 D; range, −22.0 to +7.50 D]), axial length (23.03 ± 0.96 mm [range, 19.01–26.17 mm] vs. 23.25 ± 1.14 mm [range, 18.96–30.88 mm]), and mean AL/CC ratio (2.94 ± 0.11 vs. 3.05 ± 0.13). Since the same examiner (YG) evaluated the parapapillary zones in both studies and since the supervising panel (LX, JBJ) consisted of the same members, it is unlikely that the marked difference in the prevalence of beta zone between both Chinese groups of different age was mainly due to a measurement artifact. 4 Since the participants of the present study were still children (mean age: 7.8 ± 1.7 years; range, 5–13 years), one may assume that the present study population at higher age will eventually have a markedly more myopic refractive error than the elderly Beijing Eye Study population has at its older age now. If beta zone prevalence is already now markedly higher in the young population of the present study, one may infer that beta zone may be a forerunner of the eventual final myopization. Since the genetic background may not have changed markedly, the myopic shift observed nowadays in the young generation in the Chinese metropolitan regions may be most likely due to the change in living conditions, with a more rural lifestyle for former generations and more urban lifestyle for the young generations of today. 28 This assumption fits with the hypothesis that beta zone may be associated with the lifestyle-related (i.e., more indoors studying time) increase in myopia. Correspondingly, a recent study by Park and colleagues 29 has examined and followed up myopic children with or without optic disc tilting for 5 years and has found that myopic progression is significantly greater in the tilted optic disc group than in the nontilted disc group. Optic disc tilting is usually associated with a larger parapapillary beta zone. 
Potential limitations of our study should be mentioned. First, the study was not population based so that the possibility of a selection bias existed. Second, refractometry was not performed under cycloplegic conditions, so that involuntary accommodation during refractometry may have covered latent hyperopia. Instead of cycloplegic refractometry, we measured axial length and corneal curvature and took the ratio of both parameters as surrogate for refractive error. Since the ophthalmoscopic parapapillary beta zone is more directly related to the myopia-related extension of the posterior globe segment than to myopic refractive error, the compromise in our study design with exchanging cycloplegic refractometric data with biometric measurements may have had the advantage of having a parameter more directly related to beta zone area. Third, we could not subdivide the ophthalmoscopic beta zone into the histologic beta zone and gamma zone, since OCT images were not available. Since all children in our study did not have glaucoma, and since myopia is associated mostly with gamma zone and less with histologic beta zone, the associations between myopia-related factors and gamma zone might have been better than with the ophthalmoscopic beta zone as sum of myopia-dependent gamma zone and glaucoma-dependent histologic beta zone. Fourth, a 1-year follow-up period may be short to determine the effect of lifestyle on ocular parameters. The follow-up data were used, however, only to support the findings based on the parameters measured at baseline. 
In conclusion, our study showed a markedly higher prevalence and larger size of parapapillary beta zone in Chinese school children than in children from Sydney or in Chinese adults in Beijing. It corresponds to the association between beta zone and myopia, and the myopic shift taking place in the young generations in East Asia. Beta zone area was associated with more indoors studying time after adjustment for axial length and other parameters. Correspondingly, a larger beta zone was associated with a more pronounced axial elongation and more indoors studying time at follow-up after adjusting for axial length. The results could indicate that parapapillary beta zone is associated with external factors–dependent development of myopia. 
Acknowledgments
Supported by the National Natural Science Foundation of China Grant 81170890 and by the National Key Technology R&D Program of the Ministry of Science and Technology Grants 2012BAH05F05 and 2013BAH19F04. The authors alone are responsible for the content and writing of the paper. 
Disclosure: Y. Guo, None; L.J. Liu, None; L. Xu, None; Y.Y. Lv, None; P. Tang, None; Y. Feng, None; J.Q. Zhou, None; M. Meng, None; J.B. Jonas, None 
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Figure
 
Scattergram showing the association between the time spent indoors with studying and the area of parapapillary beta zone.
Figure
 
Scattergram showing the association between the time spent indoors with studying and the area of parapapillary beta zone.
Table 1.
 
Associations (Univariate Analysis) Between the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Table 1.
 
Associations (Univariate Analysis) Between the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Age, y <0.001 0.21 0.04 0.02, 0.05
Sex 0.37
Maternal myopia 0.009 0.12 0.08 0.02, 0.13
Paternal myopia 0.32
Birth weight, kg 0.68
Maternal age at birth, y 0.32
Mother's occupation (blue collar/white collar) 0.08 0.09 0.06 −0.01, 0.12
Father's occupation (blue collar/white collar) 0.009 0.12 0.07 0.02, 0.13
Smoking by mother 0.58
Smoking by father 0.62
Body height, cm <0.001 0.20 0.005 0.003, 0.008
Body weight, kg 0.25
Body mass index, kg/m2 0.31
Urban/rural region of habitation 0.08 −0.08 −0.05 −0.09, 0.01
School grade <0.001 0.25 0.05 0.03, 0.07
Time spent outdoors 0.03 −0.12 −0.05 −0.09, −0.01
Time spent indoors studying <0.001 0.19 0.07 0.04, 0.10
Axial length, mm <0.001 0.33 0.10 0.08, 0.12
Corneal curvature radius, mm 0.31
Anterior chamber depth, mm <0.001 0.21 0.23 0.14, 0.32
Axial length/corneal curvature radius <0.001 0.33 0.88 0.67, 1.09
Refractive error, D <0.001 −0.35 −0.08 −0.10, −0.06
Best-corrected visual acuity 0.24
Horizontal optic disc diameter 0.04 −0.09 −0.14 −0.27, −0.01
Vertical optic disc diameter 0.46
Horizontal optic cup diameter 0.87
Vertical optic cup diameter 0.87
Table 2.
 
Associations (Univariate Analysis) Between the Logarithm of the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Table 2.
 
Associations (Univariate Analysis) Between the Logarithm of the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Age, y <0.001 0.27 0.05 0.03, 0.08
Sex 0.04 0.13 0.09 0.001, 0.17
Maternal myopia 0.005 0.18 0.13 0.04, 0.22
Paternal myopia 0.32
Birth weight, kg 0.94
Maternal age at birth, y 0.16
Mother's occupation (blue collar/white collar) 0.01 0.18 0.13 0.03, 0.23
Father's occupation (blue collar/white collar) 0.02 0.17 0.11 0.02, 0.21
Smoking by mother 0.81
Smoking by father 0.99
Body height, cm <0.001 0.34 0.010 0.006, 0.013
Body weight, kg 0.02 0.17 0.007 0.001, 0.013
Body mass index, kg/m2 0.17
Urban/rural region of habitation 0.03 −0.14 −0.10 −0.18, −0.01
School grade <0.001 0.31 0.07 0.04, 0.10
Time spent outdoors <0.001 −0.128 −0.12 −0.18, −0.05
Time spent indoors studying 0.001 0.24 0.10 0.104, 0.15
Axial length, mm <0.001 0.29 0.09 0.05, 0.13
Corneal curvature radius, mm 0.55
Anterior chamber depth, mm <0.001 0.23 0.27 0.13, 0.40
Axial length/corneal curvature radius <0.001 0.36 0.95 0.63, 1.26
Refractive error, D <0.001 −0.33 −0.08 −0.10, −0.05
Best-corrected visual acuity 0.99
Horizontal optic disc diameter 0.04 −0.13 −0.20 −0.40, −0.01
Vertical optic disc diameter 0.62
Horizontal optic cup diameter 0.05 −0.12 −0.18 −0.36, 0.00
Vertical optic cup diameter 0.13
Table 3.
 
Associations (Multivariate Analysis) Between the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters*
Table 3.
 
Associations (Multivariate Analysis) Between the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters*
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Time spent indoors 0.004 0.14 0.05 0.02, 0.09
Axial length, mm <0.001 0.22 0.07 0.04, 0.10
Refractive error (spherical equivalent), D <0.001 −0.29 −0.07 −0.09, −0.04
Vertical optic disc diameter 0.03 0.10 0.16 0.02 , 0.30
Urban/rural region of habitation 0.03 0.11 0.07 0.01, 0.14
Table 4.
 
Associations (Multivariate Analysis) Between the Logarithm of the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Table 4.
 
Associations (Multivariate Analysis) Between the Logarithm of the Area of Parapapillary Beta Zone and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Time spent indoors 0.04 0.14 0.06 0.00, 0.12
Axial length, mm 0.007 0.21 0.06 0.02, 0.11
Refractive error (spherical equivalent), D 0.007 −0.21 −0.05 −0.08, −0.01
Vertical optic disc diameter 0.02 0.16 0.27 0.04, 0.51
Table 5.
 
Associations (Univariate Analysis) Between the Time Spent Indoors With Studying and Ocular and Systemic Parameters
Table 5.
 
Associations (Univariate Analysis) Between the Time Spent Indoors With Studying and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Age, y 0.12
Sex 0.52
Maternal myopia 0.002 0.15 0.26 0.10, 0.43
Paternal myopia 0.04 0.10 0.19 0.01, 0.36
Birth weight, kg 0.39
Maternal age at birth, y 0.12
Mother's occupation (blue collar/white collar) <0.001 0.32 0.54 0.37, 0.70
Father's occupation (blue collar/white collar) <0.001 0.42 0.70 0.56, 0.85
Smoking by mother 0.07 −0.09 −0.33 −0.69, −0.03
Smoking by father 0.15
Body height, cm 0.03 0.11 0.008 0.001, 0.02
Body weight, kg 0.24
Body mass index, kg/m2 0.91
Urban/rural region of habitation <0.001 −0.48 −0.81 −0.95, −0.67
School grade 0.04 0.10 0.05 0.002, 0.11
Time spent outdoors <0.001 −0.35 −0.41 −0.53, −0.30
Axial length, mm <0.001 0.18 0.15 0.07, 0.23
Corneal curvature radius, mm 0.26
Anterior chamber depth, mm 0.006 0.13 0.40 0.12, 0.69
Axial length/corneal curvature radius <0.001 0.25 1.92 1.23, 2.62
Refractive error, D <0.001 −0.25 −0.16 −0.22, −0.11
Best-corrected visual acuity 0.50
Horizontal optic disc diameter 0.32
Vertical optic disc diameter 0.003 −0.14 −0.62 −1.04, −0.21
Horizontal optic cup diameter 0.06 −0.09 −0.33 −0.68, 0.01
Vertical optic cup diameter 0.02 −0.12 −0.40 −0.73, −0.08
Beta zone area, mm2 <0.001 0.19 0.50 0.26, 0.75
Table 6.
 
Associations (Multivariate Analysis) Between the Time Spent Indoors With Studying and Ocular and Systemic Parameters
Table 6.
 
Associations (Multivariate Analysis) Between the Time Spent Indoors With Studying and Ocular and Systemic Parameters
Parameter P Value Standardized Regression Coefficient Regression Coefficient 95% Confidence Interval
Parapapillary beta zone area, mm2 0.01 0.11 0.30 0.07, 0.54
Urban/rural region of habitation <0.001 −0.44 −0.75 −0.89, −0.61
Axial length/corneal curvature radius ratio 0.006 0.12 0.94 0.27, 1.62
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