Interocular symmetry and intermachine reproducibility measured by two different models of Cirrus optical coherence tomography

doi:10.21203/rs.3.rs-1970109/v1

Background: Optical coherence tomography (OCT) is a non-invasive, sensitive and reliable method to measure retinal axonal and neuronal changes quantitatively at a few micrometers. Spectral-domain high definition OCT (HD-OCT) has been used globally and upgraded over the years several times

Objective: This prospective study aims to compare interocular symmetry of the optic disc and macular data measured by Cirrus HD-OCT 4000 and HD-OCT 5000; to determine the intermachine reproducibility of the data from healthy subjects examined at the same visit by both HD-OCT models.

Materials and Methods: Forty-three volunteers were recruited for this study. Participants were examined with both HD-OCT 4000 and HD-OCT 5000 at the same visit. Data of optic nerve head (ONH) were acquired using ONH Cube 200 x 200 scans. Macular data were acquired using macular volume cube 512 x 128 scans.

Results: The average age of the participants was 33 ± 8.6 years. Interocular OCT parameters of ONH and macula were highly correlated between the right and left eyes regardless of HD-OCT 4000 or 5000. The average retinal nerve fiber layer (RNFL) thickness was thicker (96.67±11.19µm vs. 95.3±10.89µm, p<0.01), but average central subfield thickness (261.51±17.45µm vs. 262.51±17.39 µm, p<0.01) and average cube thickness (283.91± 13.59 µm vs. 286.55±13.09 µm, p<0.05) were thinner as measured by HD-OCT 4000 than by HD-OCT 5000. Intermachine reproducibility and reliability of the macular parameters and RNFL are good with high intraclass correlation coefficient (ICC) and low coefficient of variation (CV). Ganglion cell-inner plexiform layer (GCIPL) in the macula measured by two OCT models was close to each other with an average thickness of 85 µm and had high intermachine reproducibility with high ICC (0.993) and low CV (1.2%).

Conclusion: The interocular symmetry from both HD-OCT models was high. Intermachine reproducibility for RNFL and all macular parameters was also high. GCIPL has small intermachine differences and high reproducibility with perfect reliability. The results imply that GCIPL values measured by two HD-OCT models maybe used interchangeably.

Optical coherence tomography

interocular symmetry

intermachine reproducibility

ganglion cell-inner plexiform layer

interchangeability

Optical coherence tomography (OCT) as a noninvasive cross-sectional retinal imaging technique was introduced in the 1990s by Huang et al. (1). OCT is now a key tool in ophthalmology for diagnosing glaucoma and maculopathies and determining effective therapies(2, 3). Since 1999 after the first report of OCT findings in multiple sclerosis (MS)(4), OCT has been rapidly applied in neurology to diagnose and monitor neuroinflammation and neurodegeneration conditions via quantitative measurements of ganglion cell-inner plexiform layer (GCIPL) around the macula and retinal nerve fiber layer (RNFL) around the optic disc (5–7). Furthermore, the application of OCT in measuring RNFL thickness at a few micrometers enables us to precisely and promptly evaluate therapeutic effects on intracranial hypertension(8, 9).

Cirrus spectral domain high definition (HD)-OCT 4000 has since 2007 been used as a diagnostic device in macula and RNFL(10, 11). The model was upgraded into Cirrus 5000 in 2012 to take advantage of fast scan speed to enhance workflow efficiency and a fast tracker to compensate for blinking and eye movements(12, 13). In 2019, a more advanced Cirrus HD-OCT 6000 was released. The average speed of acquiring the complete set of six scans was 94 seconds using Cirrus 6000, 152 seconds using Cirrus 5000 and 161 seconds using Cirrus 4000(14). The quick emergence of upgraded models has improved practical processing, acquisition quality and reduced speckle noises, thereby bringing significant progress to the retinal-neuron pathophysiology. Indeed, upgraded OCT allows us to observe ten different retinal microstructures, including GCIPL and RNFL, and extracranial extension of the brain both in vivo and in real-time at the histological level. As known previously, the algorithms of available machines differ and yield different results for retinal thickness. The measures from different OCT devices are generally considered not to be interchangeable (15–18). To our knowledge, there are limited data on the interchangeability of different models of Cirrus HD-OCT (5, 14, 19). Given the high resolution and high sensibility of OCT measures at 1–10 micrometers, a few micrometers difference in examinations may bring incorrect interpretations of the results and mislead clinical direction. It is necessary to compare inter Cirrus HD-OCT reproducibility in order to evaluate the interchangeability of Cirrus-OCT models.

In this study, we compare interocular symmetry of the optic disc and macular data measured by Cirrus HD-OCT 4000 and 5000, and evaluate the intermachine reproducibility of the data from healthy subjects examined by both OCT models at the same visit.

Participants

Participants were randomly recruited in this study at the Department of Neurology, Linköping University Hospital, Sweden. The Ethical Committee of the Linköping University, Sweden approved the study. A written consent form was obtained before participation in this study. Seventy-one persons were examined in parallel with both Cirrus HD-OCT 4000 and HD-OCT 5000 during February and July of 2022. The inclusion criteria of participants in this study were people between 20 to 50 years old who gave consent for examination with two OCT models at the same visit. The exclusion criteria were as follows: 1) abnormal fundus manifestations like papilledema, swelling, or atrophy of the optic disc visualized by ophthalmoscopy; or 2) eye disorders including retinal disease, a history of intraocular surgery, glaucoma, severe cataract, or refractive errors more than ± 6 diopter. 3) history of diabetes, optic neuritis, hypertension.

Optical coherence tomography

Spectral-domain OCT examinations were performed on all participants without dilated pupils using both Cirrus HD-OCT model 4000 and model 5000 (Carl Zeiss Meditec, Dublin, CA, USA). Two OCT machines were placed in two different dark rooms, which were next to each other. Examination intervals between HD-OCT 4000 and 5000 were less than 10 minutes. The optic nerve head (ONH) was examined using ONH Cube 200 x 200 protocol to obtain measures of RNFL thickness, rim area, disc area and cup volume. Macula was examined using macular cube 512 × 128 protocol to obtain measures of central subfield thickness, cube volume, cube average thickness and GCIPL. Macular GCIPL thickness is the sum of the ganglion cell layer plus inner plexiform layer thickness. Scans were visually inspected immediately upon acquisition and repeated as necessary to satisfy criteria for acceptable scans with a signal strength of 7/10 or more (15, 20).

Statistical Analyses

Statistical analyses were performed using Statistical Package for the Social Sciences (SPSS) version 27. The Shapiro-Wilk test was used to analyze data distributions. Interocular symmetry was analyzed through interocular correlation and differences. Interocular correlation of OCT parameters between the right and left eye was examined using Pearson or Spearman tests depending on the data distribution. Interocular differences were presented using average values between both eyes, coefficient of variation (CV) and 5th and 95th percentile(16, 21). Intermachine difference were presented as the mean difference ± standard deviation (SD). A paired t-test or Wilcoxon Matched-Pair Signed Ranked test based on data distribution was performed. Intermacine reproducibility was presented as CV, intraclass correlation coefficient (ICC) and 95% confidence interval (CI). CV close to 0 and an ICC close to 1.0 were regarded as the best value (22). Scatter plot was used to visualize the correlation of both models. Reproducibility of intermachine was examined using the Bland-Altman plot (22, 23). The reproducibility coefficients were calculated as ± 2 SDs of the differences between two OCT machines against the means of OCT parameters. P value equal to or < 0.05 was considered statistically significant.

Demographic characteristics

Forty-three of 71 participants fulfilled the inclusion criteria after screening (Fig. 1). The mean age was 33 ± 8.6 years old with a range of 20 to 50 years. Twenty-eight of the participants (65%) were females.

Interocular symmetry measured by HD-OCT 4000 versus HD-OCT 5000

All ONH and macular parameters between right and left eyes were significantly correlated regardless of measures from HD-OCT 4000 or HD-OCT 5000 (Table 1). Spearman correlation coefficient for interocular symmetry was high for central subfield thickness (0.956 and 0.967), cube average thickness (0.951 and 0.942), cube volume (0.942 and 0.945), GCIPL (0.936 and 0.879) and RNFL (0.932 and 0.942) from HD-OCT 4000 and HD-OCT 5000 respectively. However, two HD-OCT models of disc area, rim area and cup volume had relatively low symmetry between the right and left eyes

OCT parameters from the right and left eyes were used to calculate CV for absolute agreement from each HD-OCT model and were used to assess interocular difference. Similar to the results of interocular symmetry, interocular CV value below 10% was seen in the five OCT parameters mentioned above. From both HD-OCT models (HD-OCT 4000 vs. 5000), interocular difference and CV was found lowest in cube volume (mean difference 0.13 vs 0.14 mm³; CV 1.6%) and cube average thickness (mean difference 3.58 vs. 3.74 µm; CV 1.6%), followed by central subfield thickness (mean difference 4.09 vs. 3.40 µm; CV 2.0% vs. 1.7), GCIPL (mean difference 1.40 vs. 1.53 µm, CV 2.4 vs. 2.9%) and RNFL (mean difference 3.58 vs. 3.02 µm, CV 4.3% vs. 4.1%) (Table 2).

The interocular difference and CV were relatively high for rim area (mean difference 0.13 vs. 0.10 mm³; CV 10.3% vs. 8.5 ) and disc area (mean difference 0.14 vs. 0.17 mm³; CV 9.8 vs.18.1%). Cup volume had the highest interocular difference and CV (mean difference 0.040 vs. 0.048 mm³; CV 157.6 vs. 207.4%).

Intermachine difference measured by HD-OCT 4000 versus HD-OCT 5000

Average RNFL thickness was thicker (96.67 ± 11.19 µm vs. 95.3 ± 10.89 µm, p < 0.01) (Table 2), but the average central subfield thickness (261.51 ± 17.45 µm vs. 262.51 ± 17.39 µm, p < 0.01) and cube average thickness (283.91 ± 13.59 µm vs. 286.55 ± 13.09 µm, p < 0.05) were thinner measured by HD-OCT 4000 than by HD-OCT 5000. Cube volume (10.26 ± 0.48 mm³ vs. 10.31 ± 0.47 mm³, p = 0.052) was smaller measured by HD-OCT 4000 than by HD-OCT 5000 without statistical significance. However, average rim area, disc area, cup volume and GCIPL did not differ significantly between two models.

Intermachine reproducibility

Intraclass correlation coefficient (ICC) and CV for an absolute agreement were calculated to assess intermachine reproducibility and reliability (Table 2). ICC values between 0 and 0.2 suggest low reliability; 0.21 and 0.4 fair reliability; 0.41 and 0.6 moderate reliability; between 0.61 and 0.8 high reliability; above 0.81 suggest almost perfect reliability. CV less than 10% was considered an acceptable reproducibility and CV less than 6% was considered as high reproducibility.

High intermachine reproducibility was found in central subfield thickness (0.9%), GCIPL (1.2%), cube average thickness (2.3%), cube volume (1.5%), RNFL (2.4%) and rim area (5.1%). Intermachine reliability expressed as ICC was greater than 0.9 for all OCT parameters, except cup volume (ICC 0.359). The highest intermachine reliability was observed in central subfield thickness (0.995), followed by GCIPL (0.993), cube volume (0.975) and RNFL (0.985). Disc area had acceptable reproducibility and reliability (CV 8.1%, ICC 0.968). However, cup volume had low intermachine reproducibility (CV 23.7%) with relatively low reliability (ICC 0.359).

Scatter plots (Fig. 2) showed the intermachine correlation of ONH and macular parameters measured by SD-OCT 4000 vs. SD-OCT 5000. In line with the interocular symmetry results,, central subfield thickness has the highest correlation between two machines (R² = 0.983), followed by GCIPL (R² = 0.972), RNFL (R² = 0.956) and cube volume (R² = 0.910).

The Bland and Altman plots (Fig. 3) showed the highest intermachine reproducibility for GCIPL with more than 97% of the average values falling within ± 2 SDs of the differences between the two OCT models. RNFL, central subfield thickness and cube volume had the same intermachine reproducibility of 95.3% of the average values falling within ± 2 SDs of the differences between the two OCT models (10, 23).

In this prospective study, we evaluate the data for interocular symmetry of ONH and macular parameters from healthy subjects using both Cirrus HD-OCT 4000 and 5000 at the same visit. Further, we compared the intermachine reproducibility of ONH and macular parameters. The correlations between right and left eyes are high, and differences between the eyes were small regardless of HD-OCT 4000 or 5000. These results are in agreement with previous studies(17, 21, 22). Intermachine reproducibility is generally high for all parameters in the macula and RNFL in the ONH. Intermachine differences in macular parameters and RNFL are small. This may imply that the interchangeability of macular parameters and RNFL measured with Cirrus HD-OCT models is feasible to a certain extent (16), but with considerations(10, 17, 24–26).

To our knowledge, there is a lack of data that compares between different HD-OCT models on such extensive OCT parameters from ONH and macula(16, 19, 27–29). OCT has been increasingly used in longitudinal studies in both ophthalmology and neurology(13, 30, 31). The results yielded from this study are valuable in revealing possibilities and limitations regarding the interchangeability of two models in clinical practice, research and clinical trials.

We found that the right and left eyes are highly symmetric in healthy eyes detected by both HD-OCT models. The ONH parameters including RNFL, rim and disc area, cup volume and macular parametersincluding central subfield thickness, cube volume, cube average thickness and GCIPL between right and left eyes are highly correlated with each other, showing minimal interocular differences. In the ONH, the highest interocular symmetric parameter was RNFL. In the macula, all the parameters showed high interocular symmetry.

Interocular symmetry of RNFL and cup volume was observed in healthy children aged 5–17 years (21), but the interocular asymmetry of rim and disc area, and GCIPL was reported a similar study by Song and Hwang. In a Swedish population-based study, interocular correlation of RNFL, rim and disc area, and cup volume were high in healthy children aged 6–15 years(22). In healthy adults, the interocular symmetry of RNFL and GICPL was high(17). Information on interocular differences in OCT parameters is important for evaluating of neuro-ophthalmic conditions(24). The peripapillary RNFL and macular GCIPL are the most commonly used OCT parameters to diagnose and monitor demyelinating optic neuritis, idiopathic intracranial hypertension, papilledema and ischemic optic neuropathies, and to evaluate therapeutic effects(5, 17, 24). Interocular differences of 5 micrometers for RNFL and 4 micrometers for GCIPL are considered robust thresholds for identifying optic nerve lesions(17). Our data from two HD-OCT models support that healthy eyes should have high interocular symmetry with small differences between the right and left eyes in the ONH and in the macula. Pathophysiological conditions should be considered when OCT reveals significant interocular asymmetry.

High intra- and inter-operator, and inter-visit reproducibility of spectral-domain OCT were reported(10, 28, 32). As intermachine reproducibility for Cirrus HD-OCT 4000 and 5000 was considered, the best reproducibility of OCT parameters was found in GCIPL. The average value of GCIPL thickness detected by the two OCT models was the same (85 µm) with a very minimal intermachine difference of 0.047 µm. This thickness was also very close to the previous results from other studies carried out with Cirrus HD-OCT 4000(5, 19). The coefficient of variation between the two OCT models was as small as 1.2% against the average value of GCIPL, which suggests excellent reproducibility(22, 23, 25). The intraclass correlation coefficient of GCIPL thickness between Cirrus HD-OCT 4000 and 5000 was significantly high (ICC 0,993) suggesting perfect reliability. In addition, the Bland and Altman plot displayed the highest intermachine reproducibility with more than 97% of all the GCIPL values falling within the limit of the agreement of the two HD-OCT models. When taken together, GCIPL thickness showed high reproducibility with perfect reliability and low difference measured by two HD-OCT models, which implies that GCIPL values measured by different OCT models may be used interchangeably(10, 26, 32).

The intermachine correlation of RNFL, central subfield thickness, cube volume and cube average thickness was significantly high when measured by the two OCT models. These parameters had the same reproducibility with 95.3% of the average values falling within ± 2 SDs of the average values from the two OCT models. These four parameters had also high ICC suggesting an excellent reliability. However, the intermachine differences in these four parameters were significant. Thus, the interchangeability of RNFL, central subfield thickness, cube volume and cube average thickness should be considered with caution, especially in a longitudinal study that determine therapeutic effect. The rim and disc area, as well as cup volume showed low reproducibility and low reliability of interchangeability in our study.

This study has a number of limitations. The sample size was modest and the study population was not based on age and gender. The population consisted of subjects with ages ranging from 20–50 years and was female dominant. A retrospective study enrolled 225 healthy eyes reveals no difference between males and females regarding GCIPL and RNFL thickness(19). However, this study showed thinner GCIPL and RNFL in older age. Further studies with a larger population, different age groups and equal gender distribution are warranted to confirm the results.

The interocular symmetry of all OCT parameters measured by both SD-OCT 4000 and 5000 is high. GCIPL has minimal intermachine differences and high reproducibility with perfect reliability for HD-OCT 4000 and 5000. The results imply that GCIPL values measured by two HD-OCT models may be used interchangeably.

Table 1. Interocular symmetry of optic disc and macular data from HD-OCT 4000 and HD-OCT 5000

HD-OCT Model 4000 (n=43)

HD-OCT Model 5000 (n=43)

Interocular correlation

Interocular difference

Interocular correlation

Interocular difference

Right eye

Left eye

Correlation

Difference

Mean ±SD

CV mean

Percentile

Right eye

Left eye

Correlation

Difference

Mean ±SD

CV mean

Percentile

5th

95^th

5th

95th

RNFL thickness, µm

97.07 ±

11.48

96.28 ±

11.28

0.932**

3.58 ± 2.32

4.3%

0.00

8.80

95.70 ±

11.24

94.91 ±

10.86

0.942**

3.02 ± 2.38

4.1%

0.00

7.60

Rim Area, mm²

1.47 ±

0.22

1.52 ±

0.25

0.774**

0.13 ± 0.10

10.3%

0.01

0.38

1.47 ±

0.22

1.50 ±

0.23

0.825**

0.10 ±

0.09

8.5%

0.01

0.24

Disc Area, mm²

1.72

(1.58-2.03)

1.8

(1.62-2.05)

0.773**

0.14 ± 0.11

9.8%

0.01

0.40

1.76

(1.55-2.06)

1.72

(1.57-2.03)

0.703**

0.17 ± 0.22

18.1%

0.00

0.52

Cup Volume, mm³

0.057

(0.020-0.173)

0.057

(0.012-0.104)

0.760**

0.040 ± 0.048

207.4%

0.00

0.15

0.053

(0.021-0.141)

0.069

(0.013-0.122)

0.771**

0.048 ± 0.072

157.6%

0.00

0.21

Central Subfield Thickness, µm

261.33 ± 17.68

261.70 ± 17.61

0.956**

4.09 ± 3.25

2.0%

0.00

10.8

262.72 ±

17.53

262.30 ±

17.54

0.967**

3.40 ± 2.90

1.7%

0.00

9.00

Cube Volume, mm³

10.26 ±

0.48

10.27 ±

0.49

0.942**

0.14 ± 0.09

1.6%

0.00

0.30

10.30 ±

0.48

10.30 ±

0.47

0.945**

0.13 ± 0.10

1.6%

0.00

0.30

Cube Average Thickness, µm

283.58 ± 13.61

284.23 ± 13.90

0.951**

3.58 ± 2.45

1.6%

0.00

8.00

286.84 ±

13.33

286.26 ±

13.23

0.942**

3.74 ± 2.57

1.6%

0.20

8.80

GCIPL, µm

85.00

(80-88)

85.00

(80-88)

0.936**

1.40 ± 1.35

2.4%

0.00

4.80

84.00

(80-88)

86.00

(80-88)

0.879**

1.53 ± 1.93

2.9%

0.00

5.00

RNFL = retinal nerve fiber layer; GCIPL = ganglion cell-inner plexiform layer; CV= coefficient of variation

** p<0.01 are according to Pearson or Spearman Bivariate Correlation test depending on data distribution. Parametric data is presented as mean ± SD and non-parametric data is presented as median and interquartile range (IQR).

Table 2. Intermachine reproducibility of optic disc and macular data from HD-OCT 4000 and HD-OCT 5000.

	Intermachine difference				Intermachine reproducibility
	HD-OCT Model 4000 (n= 43)	HD-OCT Model 5000 (n= 43)	Difference Mean ±SD	p value	CV mean	ICC	95% CI
	HD-OCT Model 4000 (n= 43)	HD-OCT Model 5000 (n= 43)	Difference Mean ±SD	p value	CV mean	ICC	Lower	Upper
RNFL thickness, µm	96.67 ± 11.19 (74 - 120.5)	95.3 ± 10.89 (74 - 117.5)	1.37 ± 2.35	0.000**	2.4%	0.985	0.958	0.993
Rim area, mm²	1.50 ± 0.22 (1.12 - 1.98)	1.49 ± 0.22 (1.10 - 1.93)	0.014 ± 0.076	0.236	5.1%	0.968	0.941	0.983
Disc area, mm²	1.76 (1.61-2.03)	1.77 (1.57-2.03)	0.030 ± 0.128	0.480	8.1%	0.953	0.914	0.975
Cup volume, mm³	0.056 (0.018-0.164)	0.055 (0.020-0.148)	0.057 ± 0.371	0.101	23.7%	0.359	0.180	0.652
Central Subfield Thickness, µm	261.51 ±17.45 (230-293.5)	262.51 ± 17.39 (230.5 - 295)	1.00 ± 2.25	0.006**	0.9%	0.995	0.989	0.998
Cube volume , mm³	10.26 ± 0.48 (9.35 -11.4)	10.31 ± 0.47 (9.4 -11.35)	0.04 ± 0.14	0.052	1.5%	0.975	0.953	0.987
Cube Average Thickness, µm	283.91 ±13.59 (259.5 -316.5)	286.55 ± 13.09 (261 - 315.5)	2.64 ± 6.63	0.013*	2.3%	0.926	0.851	0.962
GCIPL, µm	85.00 (80.5-88.00)	85.00 (81.00-88.00)	0.047 ± 0.950	0.111	1.2%	0.993	0.987	0.996

RNFL = retinal nerve fiber layer; GCIPL = ganglion cell-inner plexiform layer; CV: coeffient of variation; ICC: Intraclass correlation Coefficients*p< 0.05, **p<0.01 according to paired t-test or Wilcoxon Matched-Pair Signed Ranked Test depending on the data distribution. Parametric data is presented as mean ± SD and range. Non-parametric data is presented as median and interquartile range (IQR).

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Funding information: This study was supported by County Council of Östergötland and Linköping University Hospital, project numbers: LIO-799111, LIO-940688, LIO 941169.

Acknowledgements: The authors gratefully acknowledge support of the Faculty of Medicine and Health Sciences at Linköping University and Linköping University Hospital. Special thanks to support from Henry and Ella Margareta Ståhl Foundation.

Conflict of interest: The authors declare that they have no conflicts of interest.

Ethical approval: The study was approved by the Ethical Committee of the Linköping University, Sweden, study number 2013/1411-31.

Data availability statement: The data that are presented in the study are available from the corresponding author upon reasonable request.

No competing interests reported.

Interocular symmetry and intermachine reproducibility measured by two different models of Cirrus optical coherence tomography

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Version 1

Abstract

Figures

Background

Materials And Methods

Participants

Optical coherence tomography

Statistical Analyses

Results

Demographic characteristics

Interocular symmetry measured by HD-OCT 4000 versus HD-OCT 5000

Intermachine difference measured by HD-OCT 4000 versus HD-OCT 5000

Intermachine reproducibility

Discussion

Conclusion

Tables

References

Declarations

Additional Declarations

Status:

Version 1