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Decreases in ganglion cell layer and inner plexiform layer volumes correlate better with disease severity in schizophrenia patients than retinal nerve fiber layer thickness: Findings from spectral optic coherence tomography

Published online by Cambridge University Press:  23 March 2020

M. Celik ,
A. Kalenderoglu ,
A. Sevgi Karadag ,
O. Bekir Egilmez ,
B. Han-Almis  and
A. Şimşek
M. Celik*
Affiliation:
Adiyaman University, Psychiatry Department, Adiyaman, Turkey
A. Kalenderoglu
Affiliation:
Adiyaman University, Psychiatry Department, Adiyaman, Turkey
A. Sevgi Karadag
Affiliation:
Adiyaman University, Ophthalmology Department, Adiyaman, Turkey
O. Bekir Egilmez
Affiliation:
Adiyaman University, Psychiatry Department, Adiyaman, Turkey
B. Han-Almis
Affiliation:
Adiyaman Research and Education Hospital, Adiyaman, Turkey
A. Şimşek
Affiliation:
Adiyaman University, Ophthalmology Department, Adiyaman, Turkey
*
*Corresponding author. E-mail address: [email protected] (M. Celik).
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Abstract

Background

Optic coherence tomography (OCT) is a new, contactless and fast neuroimaging method. Previous studies have observed thinning of the retinal nerve fibre layer (RNFL) in many neurodegenerative diseases, and researchers have suggested that correlations exist between the thinning of the RNFL and the neurodegeneration detected with other imaging methods or the severity of illness. More recently, OCT has been used in patients with schizophrenia. RNFL thinning has also been detected in these patients. With more sophisticated devices, segmentation of the retina and measurements of the ganglion cell layer (GCL) and internal plexiform layer (IPL) can be performed.

Methods

We measured the RNFL thickness and the GCL and IPL volumes in 40 treatment refractory patients with schizophrenia, 41 treatment responsive refractory patients and 41 controls using spectral-OCT, and we evaluated the correlations between the disease severity and OCT measurements.

Results

The global RNFL thickness and GCL and IPL volumes were decreased in the patients with schizophrenia compared with the controls. In addition, the GCL and IPL volumes were lower in the treatment refractory patients with schizophrenia compared to the treatment responsive patients. Using parameters such as the Positive and Negative Syndrome Scale (PANSS) and Clinical Global Impression (CGI) scores, the disease duration and number of hospitalizations, correlations between the GCL and IPL volumes and disease severity were stronger than the correlations between the RNFL and the disease parameters.

Conclusion

Our findings suggest that OCT can be used to detect neurodegeneration in schizophrenia and that the GCL and IPL volumes can also be used to monitor the progression of neurodegeneration.

Keywords

SchizophreniaOptic coherence tomographyInner plexiform layerGanglion cell layer
Type
Original article
Information
European Psychiatry , Volume 32 , February 2016 , pp. 9 - 15
Copyright
Copyright © European Psychiatric Association 2016

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References

Siever, L.J., Davis, K.L.The pathophysiology of schizophrenia disorders: perspectives from the spectrum. Am J Psychiatry 2004; 161: 398–413.CrossRefGoogle ScholarPubMed
Shenton, M.E., Wible, C.G., McCarley, R.W.A review of magnetic resonance imaging studies of brain abnormalities in schizophrenia. Krishnan, K.Doraiswamy, P.Brain imaging in clinical psychiatry; New York: Marcel Dekker Inc; 1997. 297–380.Google Scholar
Wong, A.H., Van Tol, H.H.Schizophrenia: from phenomenology to neurobiology. Neurosci Biobehav Rev 2003; 27: 269–306.CrossRefGoogle ScholarPubMed
Wright, I.C., Rabe-Hesketh, S., Woodruff, P.W., David, A.S., Murray, R.M., Bullmore, E.T.Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry 2000; 157: 16–25.CrossRefGoogle Scholar
Shenton, M.E., Dickey, C.C., Frumin, M., McCarley, R.W.A review of MRI findings in schizophrenia. Schizophr Res 2001; 49: 1–52.CrossRefGoogle Scholar
Lawrie, S.M., Abukmeil, S.S.Brain abnormality in schizophrenia: a systematic and quantitative review of volumetric magnetic resonance imaging studies. Br J Psychiatry 1998; 172: 110–20.CrossRefGoogle ScholarPubMed
Arnone, D., Mcintosh, A.M., Tan, G.M.Y., Ebmeier, K.P.Meta-analysis of magnetic resonance imaging studies of the corpus callosum in schizophrenia. Schizophr Res 2008; 101: 124–32.CrossRefGoogle Scholar
Nelson, M.D., Saykin, A.J., Flashman, L.A., Riordan, H.J.Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging: a meta-analytic study. Arch Gen Psychiatry 1998; 55: 433–40.CrossRefGoogle ScholarPubMed
Harrison, P.J., Weinberger, D.R.Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol Psychiatry 2005; 10: 40–68.CrossRefGoogle ScholarPubMed
Steen, R.G., Hamer, R.M., Lieberman, J.A.Measurement of brain metabolites by 1H magnetic resonance spectroscopy in patients with schizophrenia: a systematic review and meta-analysis. Neuropsychopharmacology 2005; 30: 1949–62.CrossRefGoogle ScholarPubMed
Ellison-Wright, I., Bullmore, E.Meta-analysis of diffusion tensor imaging studies in schizophrenia. Schizophr Res 2009; 108: 3–10.CrossRefGoogle Scholar
Bangalore, S.S., Goradia, D.D., Nutche, J., Diwadkar, V.A., Prasad, K.M., Keshavan, M.S.Untreated illness duration correlates with gray matter loss in first-episode psychoses. Neuroreport 2009; 20: 729–34.CrossRefGoogle ScholarPubMed
Lieberman, J.A., Chakos, M., Wu, H., Alvir, J., Hoffman, E., Delbert, R., et al.Longitudinal study of brain morphology in first-episode schizophrenia. Biol Psychiatry; 2001; 49: 487–99.CrossRefGoogle ScholarPubMed
Pantelis, C., Velakoulis, D., McGorry, P.D., Wood, S.J., Suckling, J., Phillips, L.J., et al.Neuroanatomical abnormalities before and after onset of psychosis: a cross-sectional and longitudinal MRI comparison. Lancet; 2003; 361: 281–8.CrossRefGoogle ScholarPubMed
Sporn, A.L., Greenstein, D.K., Gogtay, N., Jeffries, N.O., Lenane, M., Gochman, P., et al.Progressive brain volume loss during adolescence in childhood-onset schizophrenia. Am J Psychiatry; 2003; 160: 2181–9.CrossRefGoogle ScholarPubMed
Huang, D., Swanson, E.A., Lin, C.P., Schuman, J.S., Stinson, W.G., Chang, W., et al.Optical coherence tomography. Science; 1991; 254: 1178–81.CrossRefGoogle ScholarPubMed
Fujimoto, J.G.Optical coherence tomography for ultrahigh resolution in vivo imaging. Nat Biotechnol 2003; 21: 1361–7.CrossRefGoogle ScholarPubMed
Schönfeldt-Lecuona, C, Kregel, T, Schmidt, A, Pinkhardt, EH, Lauda, F, Kassubek, J, et al. From imaging the brain to imaging the retina: optic coherence tomography in schizophrenia. Schizophr Bull. doi: 10.1093/schbul/sbv073.Google Scholar
Saidha, S., Syc, S.B., Ibrahim, M.A., Eckstein, C., Warner, C.V., Farrell, S.K., et al.Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain; 2011; 134: 518–33.CrossRefGoogle ScholarPubMed
He, X.F., Liu, Y.T., Peng, C., Zhang, F., Zhuang, S., Zhang, J.S.Optical coherence tomography assessed retinal nerve fiber layer thickness in patients with Alzheimer's disease: a meta-analysis. Int J Ophthalmol 2012; 5: 401–5.Google ScholarPubMed
Cetin, E.N., Bir, L.S., Sarac, G., Yaldızkaya, F., Yaylalı, V.Optic disc and retinal nerve fibre layer changes in Parkinson's disease. J Neuroophthalmol 2013; 37: 20–3.CrossRefGoogle ScholarPubMed
Balogh, Z., Benedek, G., Kéri, S.Retinal dysfunctions in schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 2008; 32: 297–300.CrossRefGoogle Scholar
Cabezon, L., Ascaso, F.J., Ramiro, P., Quintanilla, M., Gutierrez, E.L., Lobo, A.Optical coherence tomography: a window into the brain of schizophrenic patients. Acta Ophthalmol 2012;90:0.Google Scholar
Chu, E.M., Kolappan, M., Barnes, T.R., Joyce, E.M., Ron, M.A.A window into the brain: an in vivo study of the retina in schizophrenia using optical coherence tomography. Psychiatry Res 2012; 203: 89–94.CrossRefGoogle Scholar
Lee, W.W., 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: 7785–92.CrossRefGoogle ScholarPubMed
Chen, J., Lee, L.Clinical applications and new developments of optical coherence tomography: an evidence-based review. Clin Exp Optom 2007; 90: 317–35.CrossRefGoogle Scholar
Saidha, S., Syc, S.B., Durbin, M.K., Eckstein, C., Oakley, J.D., Meyer, S.A., et al.Visual dysfunction in multiple sclerosis correlates better with optical coherence tomography derived estimates of macular ganglion cell layer thickness than peripapillary retinal nerve fiber layer thickness. Mult Scler; 2011; 17(12): 1449–63.CrossRefGoogle ScholarPubMed
American Psychiatric Association Diagnostic and statistical manual of mental disorders 4th ed. Washington, DC: American Psychiatric Association; 2000 [text revision].Google Scholar
Lehman, A.F., Lieberman, J.A., Dixon, L.B., McGlashan, T.H., Miller, A.L., Perkins, D.O., et al.Practice guideline for the treatment of patients with schizophrenia, second edition. Am J Psychiatry; 2004; 161: 1–56.Google ScholarPubMed
Kay, S.R., Flszbein, A., Lewis, A.O.The Positive And Negative Syndrome Scale (PANSS) for schizophrenia. Schizophr Bull 1987; 13(2): 261–76.CrossRefGoogle Scholar
Guy, W.ECDEU assessment manual for psychopharmacology: clinical global impressions Rockwille, MD: National Institute of Mental Health; 1976.Google Scholar
Chhablani, J., Wong, I.Y., Kozak, I.Choroidal imaging: a review. Saudi J Ophthalmol 2014; 28(2): 123–8.CrossRefGoogle ScholarPubMed
Yeap, S., Kelly, S.P., Sehatpour, P., Magno, E., Garavan, H., Thakore, J.H., et al.Visual sensory processing deficits in schizophrenia and their relationship to disease state. Eur Arch Psychiatry Clin Neurosci 2008; 258: 305–16.CrossRefGoogle ScholarPubMed
Djamgoz, M.B.A., Hankins, M.W., Hirano, J., Archer, S.N.Neurobiology of retinal dopamine in relation to degenerative states of the tissue. Vision Res 1997; 37: 3509–29.CrossRefGoogle ScholarPubMed
Rebolleda, G., González-López, J.J., Muñoz-Negrete, F.J., Oblanca, N., Costa-Frossard, L., Álvarez-Cermeño, J.C.Color-code agreement among stratus, cirrus, and spectralis optical coherence tomography in relapsing-remitting multiple sclerosis with and without prior optic neuritis. Am J Ophthalmol 2013; 155: 890–7.CrossRefGoogle ScholarPubMed
Fjeldstad, C., Bemben, M., Pardo, G.Reduced retinal nerve fiber layer and macular thickness in patients with multiple sclerosis with no history of optic neuritis identified by the use of spectral domain high-definition optical coherence tomography. J Clin Neurosci 2011; 18: 1469–72.CrossRefGoogle ScholarPubMed
Garcia-Martin, E., Pueyo, V., Pinilla, I., Ara, J.R., Martin, J., Fernández, J.Fourier-domain OCT in multiple sclerosis patients: reproducibility and ability to detect retinal nerve fiber layer atrophy. Invest Ophthalmol Vis Sci 2011; 52: 4124–31.CrossRefGoogle ScholarPubMed
Rebolleda, G., García-García, A., Won Kim, H.R., Muñoz-Negrete, F.J.Comparison of retinal nerve fiber layer measured by time domain and spectral domain optical coherence tomography in optic neuritis. Eye 2011; 25: 233–8.CrossRefGoogle ScholarPubMed
Nickla, D.L., Wallman, J.The multifunctional choroid. Prog Retin Eye Res 2010; 29: 144–68.CrossRefGoogle ScholarPubMed
Meier, M.H., Shalev, I., Moffitt, T.E., Kapur, S., Keefe, R.S., Wong, T.Y., et al.Microvascular abnormality in schizophrenia as shown by retinal imaging. Am J Psychiatry 2013; 170(12): 1451–9.CrossRefGoogle ScholarPubMed
González-López, J.J., Rebolleda, G., Leal, M., Oblanca, N., Munoz-Negrete, F.J., Costa-Frossard, L., et al.Comparative diagnostic accuracy of ganglion cell-inner plexiform and retinal nerve fiber layer thickness measures by Cirrus and Spectralis optical coherence tomography in relapsing-remitting multiple sclerosis. Biomed Res Int 2014 http://dx.doi.org/10.1155/2014/128517.CrossRefGoogle ScholarPubMed
Chorostecki, J., Seraji-Bozorgzad, N., Shah, A., Bao, F., Bao, G., George, E., et al.Characterization of retinal architecture in Parkinson's disease. J Neurol Sci 2015; 355: 44–8.CrossRefGoogle ScholarPubMed
Garcia-Martin, E., Polo, V., Larrosa, J.M., Marques, M.L., Herrero, R., Martin, J., et al.Retinal layer segmentation in patients with multiple sclerosis using spectral domain optical coherence tomography. Ophthalmology 2014; 121: 573–9.CrossRefGoogle ScholarPubMed
Kupersmith, M., Mandel, G., Anderson, S., Meltzer, D., Kardon, R.Baseline and one month changes in the peripapillary retinal nerve fiber layer in acute optic neuritis: relation to baseline vision and MRI. J Neurol Sci 2011; 308: 117–23.CrossRefGoogle ScholarPubMed
Green, A.J., McQuaid, S., Hauser, S.L., Allen, I.V., Lyness, R.Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration. Brain 2010;133(Pt 6):1591–601.CrossRefGoogle ScholarPubMed
Ascaso, F.J., Rodriguez-Jimenez, R., Cabezón, L., López-Antón, R., Santabárbara, J., De la Cámara, C., et al.Retinal nerve fiber layer and macular thickness in patients with schizophrenia: Influence of recent illness episodes. Psychiatry Res 2015;229(1–2):230–6.CrossRefGoogle ScholarPubMed
Kang, U.G., Seo, M.S., Roh, M.S., Kim, Y., Yoon, S.C., Kim, Y.S.The effects of clozapine on the GSK-3-mediated signaling pathway. FEBS Lett 2004;560(1–3):115–9.CrossRefGoogle ScholarPubMed
Sutton, L.P., Rushlow, W.J.The effects of neuropsychiatric drugs on glycogen synthase kinase-3 signaling. Neuroscience 2011; 199: 116–24.CrossRefGoogle ScholarPubMed
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