Association of Sex and MDB Thickness Measurements
There was no difference in MDB thickness between males and females in the overall study population or in either subgroup, globally or in any quadrant or sector (P>0.162, Table 5).
Association of Race and MDB Thickness Measurements
Mean MDB thickness was highest among Hispanics (286.2±57.7 µm), followed by whites (283.7±44.0 µm), Asians (269.5±40.1 µm), and African Americans (258.6±57.5 µm) (P=0.011, Table 6). African Americans had the thinnest global, temporal, and inferior nasal MDB, whereas Asians had the thinnest nasal MDB, and Hispanics had the thickest MDB in all 4 regions. P-values for testing of mean equality of MDB measurements across races were P=0.011, 0.008, 0.026, 0.006 for global, temporal, inferior nasal, and nasal sections. MDB thickness in other quadrants and sectors was similar between all 4 races (P>0.051, Table 6).
Changes in MDB Thickness Adjusted for Age, Race, and Sex
A multivariate analysis was performed on MDB thickness in the overall study group (n=256), adjusted for age, race using whites as a reference group, and sex using females as a reference group. The MDB thickness decreased globally (0.84±0.19 µm/year, P<0.001), and across all quadrants and sectors with age (P<0.014, Table 7) at a higher rate after adjusting for race and sex. African Americans had thinner MDB than whites globally (P=0.003) and across the inferior, nasal, and temporal quadrants, and the inferonasal and superior temporal sectors (P=0.003, 0.028, 0.010, <0.001, 0.013, and 0.043, respectively), whereas the superior quadrant, superonasal and inferotemporal sectors were similar among African Americans and whites (P=0.095, 0.434, and 0.111, respectively). Asians also had significantly thinner MDB compared with whites in the global, nasal, and inferonasal measurements (P=0.031, <0.001, and 0.032, respectively). Hispanics had similar MDB thickness to whites globally (P=0.826) and across all quadrants and sectors (P>0.225). After adjusting for age and race, males and females had similar MDB thickness globally and in all quadrants and sectors (P>0.050) except the superotemporal sector, where males had thinner MDB (P=0.045). Age-related MDB thinning was not significantly different across all races (P>0.235).
MDB Area Measurements
The mean MDB area in the study population was 1.824±0.409 mm2 and overall average group values for the MDB area followed the ISNT rule (Table 2). In the normal subgroup A, the mean MDB area was 1.975±0.410 mm2. The superior and inferior quadrants were similar in size (0.564±0.148 and 0.562±0.137 mm2, respectively), followed by the nasal (0.493±0.144 mm2) and temporal quadrants (0.357±0.116 mm2). In subgroup B with normal disc variations, the global MDB area was 1.664±0.342 mm2. The average subgroup quadrant values followed the ISNT rule (0.487±0.137, 0.443±0.132, 0.428±0.137, and 0.305±0.084 mm2, respectively).
To our knowledge, this is the first study that describes the relationship of age, race, and sex with the 3D SD-OCT MDB neuroretinal rim parameter. On average, global MDB thickness decreases 0.84±0.19 µm per year (Table 7), with similar rates between men and women (P>0.162, Table 5). In terms of ethnic differences, African Americans had significantly thinner MDB values compared with whites (258.6±57.5 vs. 283.7±44.0 µm, P=0.003). Although differences were not significant, Hispanics had larger global MDB thickness values (286.2±57.7 µm) and Asians had thinner MDB values (269.5±40.1) compared with whites (Table 6). Since neuroretinal rim thickness measurements such as the MDB thickness and BMO-MRW may be considered diagnostically superior to area measurements, such as MDB area or BMO area, this paper’s discussion focuses on the MDB thickness.30,33,36
Like RNFL thickness measurements, MDB neuroretinal rim thickness also decreases with age (Tables 4, 7, 8). Age-related RNFL thinning has been reported to be 0.18 to 0.44 µm per year as measured by SD-OCT.10–12,17–20,37 As RNFL and MDB measure different anatomic regions and therefore have different normal mean values, comparing rates of percentage decline instead of absolute value decline would make a comparison of these 2 parameters easier. Therefore, past cross-sectional studies have reported that annual RNFL thinning ranges between 0.15% by Alasil and colleagues to 0.38% by Celebi and colleagues.12,17–20,37 Vianna et al11 reported a decline of 0.46% per year in 37 normal adults over the course of a 4-year (range: 2 to 6 y) longitudinal study. To compare MDB thickness to RNFL thickness and BMO-MRW, we converted the annual decline measured in microns into a proportion and presented it in Table 8. The MDB thickness decreased by an average annual rate of 0.25% in our 256 normal study subjects, indicating that our results on the MDB age-related thinning are in line with the existing literature on RNFL age-related thinning (Table 8).
Rates for age-related decline of the BMO-MRW neuroretinal rim parameter have been reported at 1.34 to 1.92 µm per year, similar to the MDB thinning of 0.84 µm per year reported in this study (Table 7).11,12,19 When using the same methodology as the current study to calculate rates of percentage decline, BMO-MRW studies reported a decline of 0.40% to 0.63% per year, which is higher but similar to the 0.25% decline reported in this study for global MDB thickness (Table 8).11,12,19 In a confocal scanning laser tomography (CSLT) study, Enders et al38 more recently reported a decline of 0.80 µm per year (or 0.34%/year) in adults with a large ONH, defined as having an area ≥2.45 mm2. This rate of 0.34% per year by CSLT is similar to the rate of 0.30% per year by SD-OCT in this study (Tables 7, 8). One reason for the slight difference between percentage decline for the BMO-MRW parameter (0.40% to 0.63%/year)11,12,19 and the MDB thickness parameter (0.30%/year, Tables 7, 8) may be that the BMO-MRW and MDB thickness measurements are procured differently. For example, the BMO-MRW low-density scan protocol consists of 24 radial scans, with 25 averages each, whereas the MDB parameter is derived from a high-density 3D volume scan with 193 raster lines, with 3 averages each.28,29 The definition of the disc border also differs between the BMO-MRW and the MDB thickness parameter, because the BMO is used for the BMO-MRW parameter and the termination of the RPE/BM complex is used for the MDB parameter. These data acquisition differences may have accounted for the slight difference between BMO-MRW and MDB rates of age-related decline. Nevertheless, this study and the past literature overall seems to suggest that neuroretinal rim parameters by CSLT and SD-OCT appear to have similar percentage rates of decline.
Rates of age-related neuroretinal thinning as measured by SD-OCT in this study are similar to those reported in past histologic studies, which have found a significant age-related decline in the number of RGC axons.39–42 The estimated mean nerve fiber count is around 0.97 to 1.24 million fibers,40–42 with a mean loss of around 4000 to 5400 fibers (0.32% to 0.54%) per year.39,41,42 The annual rates of thinning measured in this study, 0.253% for MDB thickness and 0.279% for MDB area (Table 8), are similar to those reported in histologic studies, which confirms the good correlation between neuroretinal MDB OCT measurements and histologic nerve fiber counts. The subtle differences between the predicted decay and the observed decay may be due to the presence of nonaxonal tissue or even blood vessel artifacts which may influence MDB calculations.33 Although future studies are needed to verify this hypothesis, MDB thickness measurements may better reflect nerve tissue loss compared with RNFL thickness measurements, because the MDB thickness measurements have a higher component of nerve to non-neuronal tissue. For example, primate histology studies indicate the MDB may be comprised of up to 94% nerve axons and only 5% astrocytes,34 whereas the RNFL is composed of at least 18% glial cells, including Muller cells and astrocytes.43 In addition, SD-OCT studies suggest that the RNFL thickness measurements may be comprised of almost 48.8% to 65.1% of non-neuronal tissue (ie, glial cells and blood vessels).44 Even though SD-OCT RNFL thickness studies have well-substantiated a “floor effect” ranging from 49.2 to 64.7 µm due to glial cells and blood vessels,28,44 future studies of MDB thickness are needed to verify that the “floor effect” for MDB measurements are indeed lower than that for RNFL thickness measurements. These future studies would further substantiate whether OCT is an accurate form of in vivo histology or not.45
Table 4 shows that rates of age-related decline in MDB thickness were similar for all quadrants and sectors except for the temporal quadrant, which did not decline with age (P=0.077). This is consistent with studies on RNFL age-related thinning, which showed that the thickness of the mean, superior, inferior, and nasal quadrants decreased with age, whereas the temporal quadrant did not.12,20,37 After adjusting for sex and race, the temporal quadrant declined significantly with age (P=0.014), but it had the slowest rate of age-related decline when analyzed for the entire study population compared with other quadrants (ie, 0.48 µm compared with 0.88 to 1.07 µm yearly, or 0.18% compared with 0.25% to 0.31% yearly, Table 7). This is similar to results in the BMO-MRW, where all quadrants declined with age and the temporal quadrant showed the slowest rate of decline.12 One possible explanation for the slower rate of age-related decline for the temporal quadrant is that it contains the papillomacular bundle, which is composed of thinner axons.41 Thus, assuming an equal loss in the number of axons across all quadrants, the temporal quadrant would display the least thinning as it has the thinnest axons to start with. Another theory is that slower axonal loss near the fovea may be an evolutionary protective mechanism to preserve central vision, which is supported by the temporal region of the ONH.37
Subjects with normal disc variation (ie, physiologic cupping) had thinner MDB values than those with normal discs (P<0.001, Table 3) and showed no significant thinning with age (P=0.955, Table 4), whereas those with normal discs showed significant MDB thinning with age across all but the temporal quadrant and the superotemporal sector (P<0.028, Table 4). Subgroup B with physiologic cupping was more myopic than subgroup A with normal discs (Table 1), which may affect MDB thickness measurements due to increased optic disc tilt or peripapillary atrophy. Subgroup B also had significantly fewer Hispanics than subgroup A (Table 1), which may have contributed to the thinner MDB measured in subgroup B compared with subgroup A, as Hispanics had the thickest MDB measurements overall (Table 6). The difference in age-related MDB decline among the 2 groups may be due to the fact that subjects with physiologic cupping have a lower mean MDB thickness. The normal variability of subjects within each subgroup may also explain the difference in age-related change, as aging may act differently on certain groups or individuals. In addition, as the main difference between normal subgroup B patients and normal subgroup A patients is the larger CDR of subgroup B, it is likely that this larger CDR may play a role in their having thinner MDBs and their having a smaller percentage decline in neuroretinal rim thickness per year (Table 8). Individuals with a larger CDR sometimes have a larger disc diameter, which means that despite having a similar number of axons, the neuroretinal rim is expected to be thinner in individuals with a larger CDR. A study by Tatham et al46 also concluded that small differences in CDR were inversely correlated with large changes in RGC count which in turn affects neuroretinal rim thickness.
In line with previous studies on RNFL thickness, our study showed that sex did not affect MDB thickness measurements (P=0.790, Table 5).17,19,20,23,47 Like our current study, the literature is also conflicted on the effect of sex on OCT measurements.48–50 Tun et al48 reported a significant relationship between BMO-MRW and sex in a normal Chinese population, with females having thicker measurements.
Table 6 shows that MDB thickness was different among races only in the global, nasal, temporal, and inferior nasal measurements (P<0.027). However, no significant difference in age-related MDB thinning was detected across races (P>0.235), which may be due to small sample size. A multivariate analysis adjusting for age and sex also showed that African Americans generally have thinner MDB thickness measurements compared with whites globally and across all but the superior quadrant (P<0.029). This is consistent with past studies that have noted thinner temporal RNFL thickness values in African Americans.18,49,51 However, Knight et al49 reported, compared with whites, African Americans had thicker mean and quadrant RNFL measurements in all but the temporal quadrant, whereas other studies have reported no significant differences in mean global RNFL thickness between African Americans and whites.18,20,51 Rhodes and colleagues found no significant difference in BMO-MRW thickness between subjects of European descent (ED) and those of African descent (AD), but reported that the RNFL was thinner in AD subjects in the temporal and superior temporal regions and thicker in the nasal, inferotemporal, inferonasal, and superior nasal regions.51 In a longitudinal study of BMO-MRW and RNFL thickness among AD and ED subjects, Bowd et al52 found no difference in baseline BMO-MRW, annual BMO-MRW thinning, RNFL thickness, or RNFL thinning in healthy subjects among the 2 groups, although they did note a faster rate of BMO-MRW thinning in AD “glaucoma suspects,” compared with their ED counterparts. Some studies have also found no significant difference in rim area among subjects of different races.49,53
Although our study found that MDB thickness values in Hispanics were similar to those of whites (P>0.225), it is difficult to say if these results are generalizable, because there were only 17 Hispanic subjects in this study, which makes it difficult to avoid type II errors. Our study also found that Asians had thinner MDB compared with whites globally, nasally, and inferonasally (P<0.033). Studies on the difference in RNFL thickness between Asians and whites were conflicted.20,50 Girkin et al18 studied RNFL thickness among 2 Asian ethnicities, Indians and Japanese, and found no difference between mean global RNFL thickness of Japanese and Indian subjects compared with those of ED or between Japanese and Indian subjects. However, the study found that subjects of Indian descent had thicker RNFL than Europeans across all quadrants, whereas subjects of Japanese descent had thicker nasal RNFL than those of ED, but were similar in all other quadrants.20 Another study, by Knight et al,49 noted that Asians had a thicker RNFL than Europeans across all quadrants except the nasal quadrant, which was similar in thickness among both groups. One possible explanation for the existence of racial differences in our study is that Hispanics, Asians, and African Americans are believed to have a larger optic disc size compared with whites.54 The MDB, which measures neuroretinal rim tissue, may be more affected by disc morphology than the RNFL, leading to differences that are not observed in the RNFL studies. Girkin et al53 also hypothesized that the lack of a significant effect of race on the diagnostic performance of SD-OCT may be due to individual differences among subjects of the same race, which may exceed the difference between multiple races. Another possible explanation may be the small sample size of nonwhites in our study (Table 1), which makes finding statistically significant differences more difficult. A post hoc power analysis revealed that our study does have sufficient power to test whether MDB thickness differences exist among all groups in the global, nasal, temporal, and inferonasal regions (power>90%). However, when comparing the 2 largest groups, African Americans and whites, we only had 74% power to detect differences in global thickness, and 97% power to detect differences in the temporal region, with all other regions falling <65% power. It is important to note that the post hoc power analysis utilized the mean MDB thickness values in the observed sample (Table 6) as the true value during the calculation, which explains why the power is highest in the regions with the largest difference between African Americans and whites.
Our study has several limitations. As with any cross-sectional study which attempts to evaluate the longitudinal effects of aging, our study results may not accurately reflect the real effects of aging, which is best evaluated in a longitudinal study. Nevertheless, this cross-sectional study still provides useful information, because a longitudinal study over many decades is not possible as SD-OCT has only been commercially available for the past decade or so. Future studies are needed with larger sample sizes of all racial subgroups, to better assess if racial differences exist between whites and other groups. No statistically significant difference in age-related decline was detected across races, which can be the result of a small sample size. We performed a power analysis which concluded that with a sample size of 256 participants, equal to the observed sample size, we have 41% power to detect such difference, whereas a sample size of 580 participants, with race proportions equal to the ones in our observed data, is needed to have 80% power. In addition, including a larger range of refractive errors would have enabled us to elucidate the effects of myopia or hyperopia on normal MDB thickness and area measurements. Another possible limitation of the study is the use of the default Spectralis pixel conversions when acquiring the images, which may vary with refraction. Therefore, a better study design would have corrected for refractive errors before acquiring the scans. Finally, future studies should account for variations in optic disc size, which can affect the size of the RPE/BM termination opening, which in turn may affect MDB neuroretinal rim thickness measurements.
In summary, this study shows that age-related decline in neuroretinal MDB thickness normally occurs at the rate of 0.71±0.19 µm each year (Table 4), which increases to 0.84±0.19 (Table 7) when adjusted for race and sex. Sex does not appear to affect MDB thickness measurements (P>0.162, Table 5). African Americans and Asians had thinner MDB neuroretinal rims compared with whites (P=0.003 and 0.031, respectively), whereas MDB thickness measurements for Hispanics were statistically similar to those of whites (P=0.826). We believe that the results of this study can better inform clinicians on how to account for the effect of normal aging when analyzing MDB thickness measurements over the years.
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Keywords:Copyright © 2019 Wolters Kluwer Health, Inc. All rights reserved.
optical coherence tomography; neuroretinal rim; optic nerve