Neuropsychological and Clinical Correlations of Optical Coherence Tomography Findings in Patients with Schizophrenia

Year 2023, , 739 - 747, 29.12.2023

Ayşe Sakallı Kani , Cansun Şahin Çam , Esra Biberoğlu Çelik , Uzay Dural , Melike Duran Dönmez , Semra Akkaya Turhan , Ebru Toker , Mesut Yıldız

https://doi.org/10.33808/clinexphealthsci.1331234

Abstract

Objective: There are increasing studies examining retinal fiber layer (RNFL) and ganglion cell layer (GCL) thinning in patients with schizophrenia. However, the results are controversial, and clinical and cognitive reflections of these findings remain unclear. With this study, we aim to examine retinal abnormalities and establish correlations with cognitive and clinical parameters.
Methods: In this cross-sectional study, we examined 29 patients with schizophrenia and 13 age and gender-matched healthy controls. All participants underwent psychometric assessment, neuropsychological tests, and optical coherence tomography (OCT) measurements. The retinal fiber layer and ganglion cell layer thickness were used as retinal parameters.
Results: Five patients dropped out during the OCT measurement process, 24 patients with schizophrenia and nine healthy controls were included in the analysis. There was no statistically significant difference between groups in measuring retinal nerve fiber layer or ganglion cell layer thicknesses. The verbal fluency test score negatively correlated with left RNFL superior ( ρ – .422, p <.05). STROOP response duration positively correlated with right RNFL on average (ρ = .551, p <.05), left RNFL on average (ρ = .498, p <.05), right RNFL superior (ρ = .507, p <.05), left RNFL superior (ρ = .461, p <.05) and right RNFL temporal values (ρ = .434, p <.05). STROOP response error was also positively correlated with right RNFL temporal thickness (ρ = .430, p <.05). STROOP response duration was positively correlated with right GCL total (ρ = .646, p <.01), right GCL superior (ρ = .658, p <.01) and right GCL inferior (ρ = .596, p <.01) thickness.
Conclusion: We did not find a significant relationship between reduced RNFL or GCL thickness and cognitive impairment. However, we had several positive correlations between cognitive task scores and RNFL and GCL thicknesses. Additionally, our study did not correlate symptom severity and clinical severity parameters with reduced RNFL or GCL thickness.

Keywords

schizophrenia, oct, retina, cognitive impairment, clinical severity

References

• Braff DL, Heaton R, Kuck J, Cullum M, Moranville J, Grant I, Zisook S. The generalized pattern of neuropsychological deficits in outpatients with chronic schizophrenia with heterogeneous Wisconsin Card Sorting Test results. Arch Gen Psychiatry 1991;48(10):891-898. DOI: 10.1001/archpsyc.1991.01810340023003.
• Kenny JT, Meltzer HY. Attention and higher cortical functions in schizophrenia. J Neuropsychiatry Clin Neurosci. 1991;3(3):269-275. DOI: 10.1176/jnp.3.3.269.
• Fett AK, Viechtbauer W, Dominguez MD, Penn DL, van Os J, Krabbendam L. The relationship between neurocognition and social cognition with functional outcomes in schizophrenia: A meta-analysis. Neurosci Biobehav Rev. 2011;35(3):573-588. DOI: 10.1016/j.neubiorev.2010.07.001.
• Santesteban-Echarri O, Paino M, Rice S, González-Blanch C, McGorry P, Gleeson J, Alvarez- Jimenez M. Predictors of functional recovery in first-episode psychosis: A systematic review and meta-analysis of longitudinal studies. Clin Psychol Rev. 2017; 58:59-75. DOI: 10.1016/j.cpr.2017.09.007.
• Van Dee V, Schnack HG, Cahn W. Systematic review and meta-analysis on predictors of prognosis in patients with schizophrenia spectrum disorders: An overview of current evidence and a call for prospective research and open access to datasets. Schizophr Res. 2023; 254:133-142. DOI: 10.1016/j.schres.2023.02.024.
• Prasannakumar A, Kumar V, Mailankody P, Appaji A, Battu R, Berendschot T, Rao NP. A systematic review and meta-analysis of optical coherence tomography studies in schizophrenia, bipolar disorder and major depressive disorder. World J Biol Psychiatry 2023:1-14. DOI: 10.1080/15622975.2023.2203231.
• Samani NN, Proudlock FA, Siram V, Suraweera C, Hutchinson C, Nelson CP, Al- Uzri M, Gottlob I. Retinal layer abnormalities as biomarkers of schizophrenia. Schizophr Bull. 2018;44(4):876-885. DOI: 10.1093/schbul/sbx130.
• Sarkar S, Rajalakshmi A, Avudaiappan S, Eswaran S. Exploring the role of macular thickness as a potential early biomarker of neurodegeneration in acute schizophrenia. International Ophthalmology 2021; 41 (8):2737-2746. DOI: 10.1007/s10792-021-01831-z.
• Huang D, Swanson EA, Lin CP, Schuman JS, Stinson WG, Chang W, Hee MR, Flotte T, Gregory K, Puliafito CA. Optical coherence tomography. Science 1991;254(5035):1178-1181. DOI:10.1126/science.1957169.
• Petzold A, de Boer JF, Schippling S, Vermersch P, Kardon R, Green A, Calabresi PA, Polman C. Optical coherence tomography in multiple sclerosis: A systematic review and meta-analysis. Lancet Neurol. 2010;9(9):921-932. DOI:10.1016/s1474-4422(10)70168-x.
• Inzelberg R, Ramirez JA, Nisipeanu P, Ophir A. Retinal nerve fiber layer thinning in Parkinson disease. Vision Res. 2004;44(24):2793-2797. DOI: 10.1016/j.visres.2004.06.009.
• Katsimpris A, Karamaounas A, Sideri AM, Katsimpris J, Georgalas I, Petrou P. Optical coherence tomography angiography in Alzheimer's disease: A systematic review and meta-analysis. Eye (Lond.) 2022;36(7):1419-1426. DOI: 10.1038/s41433-021-01648-1.
• Kazakos CT, Karageorgiou V. Retinal changes in schizophrenia: A systematic review and meta-analysis based on individual participant data. Schizophr Bull. 2020;46(1):27-42. DOI:10.1093/schbul/sbz106.
• Pan J, Zhou Y, Xiang Y, Yu J. Retinal nerve fiber layer thickness changes in schizophrenia: A meta-analysis of case-control studies. Psychiatry Res. 2018; 270:786-791. DOI: 10.1016/j.psychres.2018.10.075.
• Lizano P, Bannai D, Lutz O, Kim LA, Miller J, Keshavan M. A meta-analysis of retinal cytoarchitectural abnormalities in schizophrenia and bipolar disorder. Schizophr Bull. 2020;46(1):43-53. DOI:10.1093/schbul/sbz029.
• Kaya H, Ayık B, Tasdelen R, Sevimli N, Ertekin E. Comparing retinal changes measured by optical coherence tomography in patients with schizophrenia and their siblings with healthy controls: Are retinal findings potential endophenotype candidates? Asian J Psychiatr. 2022; 72:103089. DOI: 10.1016/j.ajp.2022.103089.
• Kurtulmus A, Sahbaz C, Elbay A, Guler EM, Sonmez Avaroglu G, Kocyigit A, Ozdemir MH, Kirpinar I. Clinical and biological correlates of optical coherence tomography findings in schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2023. DOI: 10.1007/s00406-023-01587-w.
• Kostakoglu A, Batur S, Tiryaki A, Gogus A. Reliability and validity of the Turkish version of the Positive and Negative Syndrome Scale (PANSS). Türk Psikoloji Dergisi 1999;14(44). (Turkish)
• Wechsler D. Wechsler Memory Scale-Revised. San Antonio. Harcourt Brace Jovanovich; 1987.
• Golden C, Freshwater SM, Golden Z. Stroop color and word test: A manual for clinical and experimental uses. Chicago, IL: Stoelting Co; 1978.
• Reitan RM. Validity of the Trail Making Test as an indicator of organic brain damage. Perceptual and Motor Skills 1958;8(3):271-276.
• Piatt AL, Fields JA, Paolo AM, Tröster AI. Action (verb naming) fluency as an executive function measure: Convergent and divergent evidence of validity. Neuropsychologia 1999;37(13):1499-1503.
• Bingöl A, Eroğlu G, Haktanır I. Türk toplumunda sözel akıcılık becerisi; Bir standardizasyon çalışması. 15. Ulusal Nöroloji Kongresi, 1994. (Turkish)
• Ascaso FJ, Laura C, Quintanilla MÁ, Gutiérrez Galve L, López-Antón R, Cristóbal JA, Lobo A. Retinal nerve fiber layer thickness measured by optical coherence tomography in patients with schizophrenia: A short report. Eur J Psychiatry 2010;24(4):227-235.
• Chu EM-Y, Kolappan M, Barnes TR, Joyce EM, Ron MA. A window into the brain: An in vivo study of the retina in schizophrenia using optical coherence tomography. Psychiatry Research: Neuroimaging 2012;203(1):89-94. DOI: 10.1016/j.pscychresns.2011.08.011.
• Kurtulmus A, Elbay A, Parlakkaya FB, Kilicarslan T, Ozdemir MH, Kirpinar I. An investigation of retinal layer thicknesses in unaffected first-degree relatives of schizophrenia patients. Schizophr Res. 2020; 218:255-261. DOI: 10.1016/j.schres.2019.12.034.
• Silverstein SM, Paterno D, Cherneski L, Green S. Optical coherence tomography indices of structural retinal pathology in schizophrenia. Psychol Med. 2018;48(12):2023-233. DOI:10.1017/s0033291717003555.
• Lee WW, Tajunisah I, Sharmilla K, Peyman M, Subrayan V. Retinal nerve fiber layer structure abnormalities in schizophrenia and its relationship to disease state: Evidence from optical coherence tomography. Invest Ophthalmol Vis Sci. 2013;54(12):7785-7792. DOI:10.1167/iovs.13-12534.
• Ascaso FJ, Rodriguez-Jimenez R, Cabezón L, López-Antón R, Santabárbara J, De la Cámara C, Modrego PJ, Quintanilla MA, Bagney A, Gutierrez L, Cruz N, Cristóbal JA, Lobo A. Retinal nerve fiber layer and macular thickness in patients with schizophrenia: Influence of recent illness episodes. Psychiatry Res. 2015;229(1-2):230-236. DOI: 10.1016/j.psychres.2015.07.028.
• Van Koolwijk LM, Despriet DD, Van Duijn CM, Oostra BA, Van Swieten JC, de Koning I, Klaver CCW, Lemij HG. Association of cognitive functioning with retinal nerve fiber layer thickness. Invest Ophthalmol Vis Sci. 2009;50(10):4576-4580. DOI:10.1167/iovs.08-3181.
• Liu Y, Huang L, Tong Y, Chen J, Gao D, Yang F. Association of retinal nerve fiber abnormalities with serum CNTF and cognitive functions in schizophrenia patients. Peer J. 2020;8: e9279. DOI: 10.7717/peerj.9279.
• Liu Y, Chen J, Huang L, Yan S, Bian Q, Yang F. Relationships among retinal nerve fiber layer thickness, vascular endothelial growth factor, and cognitive impairment in patients with schizophrenia. Neuropsychiatr Dis Treat. 2021; 17:3597-3606. DOI: 10.2147/ndt. S336077.
• Topcu-Yilmaz P, Aydin M, Cetin Ilhan B. Evaluation of retinal nerve fiber layer, macular, and choroidal thickness in schizophrenia: Spectral optic coherence tomography findings. Psychiatry and Clinical Psychopharmacology 2019;29(1):28-33. DOI:10.1080/24750573.2018.1426693.
• Bannai D, Lizano P, Kasetty M, Lutz O, Zeng V, Sarvode S, Kim LA, Hill S, Tamminga C, Clementz B, Gershon E, Pearlson G, Miller JB, Keshavan M. Retinal layer abnormalities and their association with clinical and brain measures in psychotic disorders: A preliminary study. Psychiatry Res Neuroimaging 2020; 299:111061. DOI: 10.1016/j.pscychresns.2020.111061.