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Influence of Eye Biometrics and Corneal Micro-Structure on Noncontact Tonometry

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Influence of Eye Biometrics and Corneal Micro-Structure on Noncontact Tonometry RESEARCH ARTICLE Influence of eye biometrics and corneal micro-structure on noncontact tonometry Danilo A. Jesus1*, Maøgorzata Majewska1, Patrycja Krzyżanowska-Berkowska2, D. Robert Iskander1 1 Department of Biomedical Engineering, Wroclaw University of Science & Technology, Wroclaw, Poland, 2 Department of Ophthalmology, Wroclaw Medical University, Wroclaw, Poland * [email protected] a1111111111 a1111111111 Abstract a1111111111 a1111111111 a1111111111 Purpose Tonometry is widely used as the main screening tool supporting glaucoma diagnosis. Still, its accuracy could be improved if full knowledge about the variation of the corneal bio- OPEN ACCESS mechanical properties was available. In this study, Optical Coherence Tomography (OCT) Citation: Jesus DA, Majewska M, Krzyżanowska- speckle statistics are used to infer the organisation of the corneal micro-structure and Berkowska P, Iskander DR (2017) Influence of eye biometrics and corneal micro-structure on hence, to analyse its influence on intraocular pressure (IOP) measurements. noncontact tonometry. PLoS ONE 12(5): e0177180. https://doi.org/10.1371/journal. pone.0177180 Methods Editor: Sanjoy Bhattacharya, Bascom Palmer Eye Fifty-six subjects were recruited for this prospective study. Macro and micro-structural cor- Institute, UNITED STATES neal parameters as well as subject age were considered. Macro-structural analysis included Received: January 17, 2017 the parameters that are associated with the ocular anatomy, such as central corneal thick- Accepted: April 23, 2017 ness (CCT), corneal radius, axial length, anterior chamber depth and white-to-white corneal Published: May 4, 2017 diameter. Micro-structural parameters which included OCT speckle statistics were related Copyright: © 2017 Jesus et al. This is an open to the internal organisation of the corneal tissue and its physiological changes during life- access article distributed under the terms of the time. The corneal speckle obtained from OCT was modelled with the Generalised Gamma Creative Commons Attribution License, which (GG) distribution that is characterised with a scale parameter and two shape parameters. permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are Results within the paper and its Supporting Information In macro-structure analysis, only CCT showed a statistically significant correlation with IOP file. (R2 = 0.25, p<0.001). The scale parameter and the ratio of the shape parameters of GG dis- Funding: This work was supported by the Marie tribution showed statistically significant correlation with IOP (R2 = 0.19, p<0.001 and R2 = Curie Innovative Training Networks, Ageing Eye, 0.17, p<0.001, respectively). For the studied group, a weak, although significant correlation AGEYE, 608049 and partially funded by National 2 Science Centre, Poland, Grant No: 2014/15/B/ST7/ was found between age and IOP (R = 0.053, p = 0.04). Forward stepwise regression 05220. showed that CCT and the scale parameter of the Generalised Gamma distribution can be 2 Competing interests: The authors have declared combined in a regression model (R = 0.39, p<0.001) to study the role of the corneal struc- that no competing interests exist. ture on IOP. PLOS ONE | https://doi.org/10.1371/journal.pone.0177180 May 4, 2017 1 / 15 Corneal micro-structure and IOP Conclusions We show, for the first time, that corneal micro-structure influences the IOP measurements obtained from noncontact tonometry. OCT speckle statistics can be employed to learn about the corneal micro-structure and hence, to further calibrate the IOP measurements. Introduction Glaucoma is the leading cause of global irreversible blindness [1]. It affects more than 70 mil- lion people worldwide and it is estimated to reach 111.8 million in 2040 [2]. Although the pathogenesis of glaucoma is not fully understood, the increased level of intraocular pressure (IOP) has been clearly linked to a progressive degeneration of retinal ganglion cells [3,4]. Intraocular pressure is routinely assessed by applanation tonometry and its normal level ranges from about 10 to 21 mmHg [5]. The accuracy of applanation tonometry is influenced by corneal stiffness that varies with a number of parameters, such as thickness, curvature and age [6]. The influence of the central corneal thickness (CCT) on IOP measurements has been assessed in several studies in a relationship that has not been precisely specified. A number of corrections has been presented in the literature ranging from 0.12 mmHg/0.01mm to 1 mmHg/ 0.01mm of corneal thickness [7±9]. It is well known that for healthy eyes non-corrected IOP is underestimated in thinner corneas and overestimated in thicker ones. The relationship between anterior corneal radius (CR) and IOP has also been studied [10,11]. Unlike CCT, the effect of CR is small and limited to a range between 0.57 mmHg/1mm to 1.14 mmHg/1mm [6]. Both CCT and CR may be viewed as corneal macro-structural parameters that influence the accuracy of applanation tonometry. However, in vitro experiments [12,13] and theoretical models [14] have shown that the cornea exhibits mechanical and viscoelastic properties. This may explain the wide range obtained for CCT correction and indicate that the macro-structure described by CCT and CR only partially explains the variance of IOP whereas other properties, related to the micro-structure of the cornea, may also contribute [15]. Cornea is found to increase its stiffness as the characteristics of viscoelastic behaviour decrease with age [16,17]. Such changes in corneal micro-structure contribute to a variation of corneal biomechanical variables which may be independent of CCT or IOP. However, the assessment of the micro-structure effect in corneal tissue stiffness was limited to few studies [10] due to the lack of means to measure it in vivo. Spoerl et. al [7] suggested that the measured IOP should be corrected by the CCT and an age-dependent correction factor, pointing that an increase of corneal thickness in a young person has a lower influence on the measured IOP than the same increase of thickness in an older subject. Despite the assumption made by Spoerl et. al [7], ageing is not necessarily a linear process and may differently affect each subject. Parameters such as medical history (i.e., diabetes or topical drugs), ocular anatomy, sun exposure, alimentation or ethnicity may all play a role in that process [18,19]. Moreover, the actual correction does not apply to other factors such cor- neal swelling, wound healing, and diseases such as keratoconus that all have possible effect on corneal micro-structure and hence, subsequently, on the IOP measurements. Therefore, new techniques are needed to measure in vivo the contribution of the corneal micro-structure on the IOP measurement. Optical Coherence Tomography (OCT) has become a popular instrument to visualise the anterior eye. It is based on interferometry which gives rise to speckleÐa form of noise origi- nating from the backscattered light that degrades the quality of OCT image. However, speckle PLOS ONE | https://doi.org/10.1371/journal.pone.0177180 May 4, 2017 2 / 15 Corneal micro-structure and IOP also has a signal-carrying component [20] which can be used to infer the micro-structure of the corneal tissue. The texture analysis of the OCT speckle to characterize biological tissues in vivo has already been applied in different contexts such as, to differentiate between normal and tumour tissues [21], in diabetic retinopathy characterization [22] and retinal segmentation [23]. Our previous studies have shown that corneal speckle acquired by OCT is also sensitive to micro-structural changes in cornea [24]. Therefore, in this study, the hypothesis was that IOP measurements obtained from noncon- tact tonometry are influenced by the micro-structure of the cornea. The contribution of the corneal structure on IOP measurements before and after its correction using CCT was explored. Corneal speckle statistics obtained from OCT were used to infer the corneal micro- structure whereas, the macro-structure was analysed using CCT and CR. Subject age was also considered. In addition, other biometric parameters including axial length (AL), anterior chamber depth (ACD) and white-to-white (WTW) corneal diameter were considered for the macro-structure analysis. Methods This is a prospective study that included 56 Caucasian subjects (25 male and 31 female) with a refractive error smaller than 1 Dioptre. A medical history review has been conducted prior to measurements. Only subjects without any reported eye disease were considered. All subjects underwent thorough OCT examination, along standard examination with a biomicroscope, to ensure that their corneas were normal. The number of subjects was sufficient to detect changes of, at least, 6.6% in the mean value of any parameter with power of 1 − β = 99% at α = 5% level of significance according to the following sample size calculation formula [25]: ðtð1 À a; N À 2Þ þ tð1 À b; N À 2ÞÞ2 n ¼ s2 ðDmÞ2 The mean (± standard deviation) age of the participants was 44.7 (± 19.3) years; range from 22 to 78. The study design was approved by the Bioethical Committee of the Wroclaw Medical University (No 332/215). All subjects were treated in accordance with the principles of the Declaration of Helsinki. All subjects provided written informed consent after the goals of the research and consequences of participation had been discussed. Matlab (Mathworks, Natick, MA) was used to develop the algorithm and the statistical analysis, which included the non- parametric Wilcoxon test, the two-sample Kolmogorov-Smirnov test, the coefficient of deter- mination, the linear regression and the multilinear forward step-wise regression analysis based on linear least squares. In this study, only the right eye of each subject was assessed and measured. Data acquisition A spectral domain OCT (SOCT, Copernicus HR, Optopol, Poland) was used to acquire images of the cornea. The signal source was a super luminescent diode with a centre wavelength of 850 nm, and axial and lateral resolution of 3 μm and 15 μm, respectively.
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