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Loss of temporal retinal nerve fibers in Parkinson disease: a mitochondrial pattern?
Abstract
BACKGROUND AND PURPOSE: Optic nerve involvement is frequent in mitochondrial disease, and retinal abnormalities are described in Parkinson's disease (PD). METHODS: We evaluated retinal nerve fiber layer (RNFL) thickness by optical coherence tomography in 43 patients with PD and in 86 age-matched controls. We considered separately the eyes ipsilateral and contralateral to the most affected body side in patients with PD. ancova analysis, Pearson test, and multiple regression analysis were used (P < 0.05). RESULTS: Patients with PD showed significantly thinner temporal RNFL thickness compared to controls (P = 0.004), more evident in the eye contralateral to the most affected body side. Average RNFL thickness significantly correlated with age in both controls and patients with PD (P-values ranging from 0.001 to 0.019), whereas in patients with PD RNFL thickness did not correlate with clinical variables. CONCLUSIONS: Our study reveals a loss of retinal nerve fibers in the temporal quadrant in PD, which is typically susceptible in mitochondrial optic neuropathies.
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“Moreover, abnormalities in visual function have been reported (Bodis-Wollner, 1990; Nowacka et al., 2014) in PD patients and correlated with changes in retinal tissue (La Morgia et al., 2013; Yu et al., 2014) (Table 1).”
From The role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma. (2017) · cites this paper as La Morgia et al., 2013
Citations
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ResultInner Retinal Layer Thinning in Parkinson Disease
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Cited by
Sorted by citations
Visual dysfunction in Parkinson’s disease
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“Interocular differences are seen in retinal thickness in Parkinson’s disease (Shrier et al., 2012) with more thinning contralateral to the side of motor symptoms (La Morgia et al., 2013), consistent with an asymmetric process involving the eye on the same side as the affected substantia nigra.”
BackgroundResultThe role of microglia in retinal neurodegeneration: Alzheimer’s disease, parkinson, and glaucoma.
Ramirez, A. I., de Hoz, R., Salobrar-Garcia, E., Salazar, J. J., Rojas, B., Ajoy, D., López-Cuenca, I., Rojas, P., Triviño, A., & Ramírez, J. M. (2017) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2017.00214 · Cited by 466
“Moreover, abnormalities in visual function have been reported (Bodis-Wollner, 1990; Nowacka et al., 2014) in PD patients and correlated with changes in retinal tissue (La Morgia et al., 2013; Yu et al., 2014) (Table 1).”
BackgroundRetinal Nerve Fiber Layer Thickness Changes in Parkinson Disease: A Meta-Analysis
Yu, J.-G., Feng, Y.-F., Xiang, Y., Huang, J.-H., Savini, G., Parisi, V., Yang, W.-J., & Fu, X.-A. (2014) · PLoS ONE · doi:10.1371/journal.pone.0085718 · Cited by 200
“Two studies were done in Greece [5,21], 3 in Turkey [6,19,23], 2 in Spain [17,24], 1 each in Iran [20], Italy [22], USA [9], United Kingdom [7], Israel [18] and Germany [4].”
BackgroundPast, present and future role of retinal imaging in neurodegenerative disease
Kashani, A. H., Asanad, S., Chan, J. W., Singer, M., Zhang, J., Sharifi, M., Khansari, M. M., Abdolahi, F., Shi, Y., Biffi, A., et al. (2021) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2020.100938 · Cited by 169
García‐Martín, E., Larrosa, J. M., Polo, V., Satué, M., Marques, M. L., Alarcia, R., Seral, M., Fuertes, I., Otín, S., & Pablo, L. E. (2013) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2013.09.028 · Cited by 155
“A recent improvement in OCT technology is the prototype of specific software that allows for automatic differentiation and quantification of the 10 retinal layers using the Spectralis OCT.”
BackgroundInfluentialOcular and visual disorders in Parkinson's disease: Common but frequently overlooked
Ekker, M. S., Janssen, S., Seppi, K., Poewe, W. H., de Vries, N. M., Theelen, T., Nonnekes, J. H., & Bloem, B. R. (2017) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2017.02.014 · Cited by 154
Multimodal brain and retinal imaging of dopaminergic degeneration in Parkinson disease
Lee, J., Martín‐Bastida, A., Murueta‐Goyena, A., Gabilondo, I., Cuenca, N., Piccini, P. P., & Jeon, B. (2022) · Nature Reviews Neurology · doi:10.1038/s41582-022-00618-9 · Cited by 132
Morgia, C. L., Vito, L. D., Carelli, V., & Carbonelli, M. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00710 · Cited by 132
“Interestingly, as for the RNFL results reported by OCT studies (42), it has been described an interocular asymmetry for the foveal thickness, pointing again to an asymmetry of the neurodegenerative process in PD, congruent with the motor symptoms of the disease (61).”
BackgroundResultRetinal thinning and correlation with functional disability in patients with Parkinson's disease
Satué, M., Seral, M., Otín, S., Alarcia, R., Herrero, R., BAMBO, M., FUERTES, M., Pablo, L. E., & García‐Martín, E. (2013) · British Journal of Ophthalmology · doi:10.1136/bjophthalmol-2013-304152 · Cited by 130
Chrysou, A., Jansonius, N. M., & van Laar, T. (2019) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2019.04.023 · Cited by 130
Satué, M., Obís, J., Rodrigo, M. J., Otín, S., Fuertes, M. I., Viladés, E., Gracia, H., Ara, J. R., Alarcia, R., Polo, V., et al. (2016) · Journal of Ophthalmology · doi:10.1155/2016/8503859 · Cited by 126
“Contrary to macular measurements, correlations between disease severity/duration and pRNFL thickness have proved to be scarce or nonexistent [55, 57].”
BackgroundElectrophysiology and Optical Coherence Tomography to Evaluate Parkinson Disease Severity
García‐Martín, E., Mena, D. R., Satué, M., Almárcegui, C., Dolz, I., Alarcia, R., Seral, M., Polo, V., Larrosa, J. M., & Pablo, L. E. (2014) · Investigative Ophthalmology & Visual Science · doi:10.1167/iovs.13-13062 · Cited by 127
Satué, M., García‐Martín, E., Fuertes, I., Otín, S., Alarcia, R., Herrero, R., BAMBO, M., Pablo, L. E., & Fernández, F. J. F. (2013) · Eye · doi:10.1038/eye.2013.4 · Cited by 115
Retinal Ganglion Cells and Circadian Rhythms in Alzheimer’s Disease, Parkinson’s Disease, and Beyond
Morgia, C. L., Ross‐Cisneros, F. N., Sadun, A. A., & Carelli, V. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00162 · Cited by 116
Optic neuropathies: the tip of the neurodegeneration iceberg
Carelli, V., Morgia, C. L., Ross‐Cisneros, F. N., & Sadun, A. A. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx273 · Cited by 116
“onstrated by selective RNFL thinning in the temporal sector (24,131,132).”
BackgroundRetinal α-synuclein deposits in Parkinson’s disease patients and animal models
Veys, L., Vandenabeele, M., Ortuño‐Lizarán, I., Baekelandt, V., Cuenca, N., Moons, L., & Groef, L. D. (2019) · Acta Neuropathologica · doi:10.1007/s00401-018-01956-z · Cited by 114
Vujosevic, S., Parra, M. M., Hartnett, M. E., O’Toole, L., Nuzzi, A., Limoli, C., Villani, E., & Nucci, P. (2022) · Eye · doi:10.1038/s41433-022-02056-9 · Cited by 109
Photoreceptor layer thinning in idiopathic Parkinson's disease
Roth, N. M., Saidha, S., Zimmermann, H. G., Brandt, A. U., Isensee, J., Benkhellouf‐Rutkowska, A., Dornauer, M., Kühn, A. A., Müller, T. H., Calabresi, P. A., et al. (2014) · Movement Disorders · doi:10.1002/mds.25896 · Cited by 105
Optical Coherence Tomography Angiography in Neurodegenerative Diseases: A Review
Tsokolas, G., Tsaousis, K. T., Diakonis, V. F., Matsou, A., & Tyradellis, S. (2020) · Eye and Brain · doi:10.2147/eb.s193026 · Cited by 104
The optic nerve: A “mito-window” on mitochondrial neurodegeneration
Maresca, A., Morgia, C. L., Caporali, L., Valentino, M. L., & Carelli, V. (2012) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2012.08.004 · Cited by 97
Oculo‐visual abnormalities in Parkinson's disease: Possible value as biomarkers
Guo, L., Normando, E. M., Shah, P. A., Groef, L. D., & Cordeiro, M. F. (2018) · Movement Disorders · doi:10.1002/mds.27454 · Cited by 89
“Intriguingly, OCT examinations have revealed that the temporal quadrant of the retina seems to be more affected in PD,(97,152,154,155,157,158) which is a disease feature that has also been described in Leber’s hereditary optic neuropathy, the first human disease to be associated with mitochondrial DNA defects.(10,11,1…”
BackgroundResultInfluentialPolo, V., Satué, M., Rodrigo, M. J., Otín, S., Alarcia, R., BAMBO, M., FUERTES, M., Larrosa, J. M., Pablo, L. E., & García‐Martín, E. (2016) · BMJ Open · doi:10.1136/bmjopen-2015-009658 · Cited by 83
Optical coherence tomography as a tool to evaluate retinal changes in Parkinson's disease
Mailankody, P., Battu, R., Khanna, A., Lenka, A., Yadav, R., & Pal, P. K. (2015) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2015.08.002 · Cited by 82
Optical Coherence Tomography Angiography in Neurodegenerative Disorders
Pellegrini, M., Vagge, A., Desideri, L. F., Bernabei, F., Triolo, G., Mastropasqua, R., Noce, C. D., Borrelli, E., Sacconi, R., Iovino, C., et al. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9061706 · Cited by 82
Remodeling of the fovea in Parkinson disease
Spund, B., Ding, Y., Liu, T., Selesnick, I., Glazman, S., Shrier, E. M., & Bodis-Wollner, I. G. (2012) · Journal of Neural Transmission · doi:10.1007/s00702-012-0909-5 · Cited by 71
Retinal correlates of neurological disorders
Yap, T. E., Balendra, S. I., Almonte, M. T., & Cordeiro, M. F. (2019) · Therapeutic Advances in Chronic Disease · doi:10.1177/2040622319882205 · Cited by 73
Retinal Thickness and Microvascular Pattern in Early Parkinson's Disease
Rascunà, C., Russo, A., Terravecchia, C., Castellino, N., Avitabile, T., Bonfiglio, V. M. E., Fallico, M., Chisari, C. G., Cicero, C. E., Grillo, M., et al. (2020) · Frontiers in Neurology · doi:10.3389/fneur.2020.533375 · Cited by 61
“Several OCT studies reported a peripapillary RNFL thinning in PD patients as compared to HCs (29, 30).”
ResultVenturing into the no‐man's land of the retina in Parkinson's disease
Bodis-Wollner, I. G., Miri, S., & Glazman, S. (2013) · Movement Disorders · doi:10.1002/mds.25741 · Cited by 60
“La Morgia et al.(27) reported that RNFL thinning was more evident in the eye contralateral to the most affected body side.”
BackgroundInfluentialCorneal nerve microstructure in Parkinson’s disease
Misra, S. L., Kersten, H. M., Roxburgh, R. H., Danesh-Meyer, H. V., & McGhee, C. N. J. (2017) · Journal of Clinical Neuroscience · doi:10.1016/j.jocn.2017.02.033 · Cited by 59
Roth, N. M., Saidha, S., Zimmermann, H. G., Brandt, A. U., Oberwahrenbrock, T., Maragakis, N. J., Tumani, H., Ludolph, A. C., Meyer, T., Calabresi, P. A., et al. (2013) · European Journal of Neurology · doi:10.1111/ene.12146 · Cited by 58
Does retina play a role in Parkinson's Disease?
Devi, S. M., Iyer, M., Aswathy, N. P., Dhivya, V., & Vellingiri, B. (2020) · Acta Neurologica Belgica · doi:10.1007/s13760-020-01274-w · Cited by 56
Dopamine, Alpha-Synuclein, and Mitochondrial Dysfunctions in Parkinsonian Eyes
Indrieri, A., Pizzarelli, R., Franco, B., & Leonibus, E. D. (2020) · Frontiers in Neuroscience · doi:10.3389/fnins.2020.567129 · Cited by 57
“…et al., 2013; La Morgia et al., 2013; Moreno-Ramos et al., 2013; Bodis-Wollner et al., 2014b; Lee et al., 2014a; Satue et al., 2016; Aydin et al., 2018; Matlach et al., 2018) that, notably, is typically affected in mitochondrial optic neuropathies (La Morgia et al., 2013; Maresca et al., 2013).”
BackgroundInner retinal thinning as a biomarker for cognitive impairment in de novo Parkinson’s disease
Sung, M. S., Choi, S., Kim, J.-H., Ha, J. Y., Kim, B. C., Heo, H., & Park, S. W. (2019) · Scientific Reports · doi:10.1038/s41598-019-48388-7 · Cited by 54
Andrade, C., Beato, J. N., Monteiro, A., da Costa, A. G., Penas, S. C., Guimarães, J., Falcão‐Reis, F., & Garrett, C. (2016) · Movement Disorders · doi:10.1002/mds.26486 · Cited by 51
“supported the involvement of the retina in PD.(13,14,16,17,25) These findings may have several clini-”
BackgroundMoschos, M. M., & Chatziralli, I. (2017) · Seminars in Ophthalmology · doi:10.1080/08820538.2017.1307423 · Cited by 50
Retina Thickness as a Marker of Neurodegeneration in Prodromal Lewy Body Disease
Lee, J., Ahn, J., Oh, S., Shin, J. Y., Kim, Y. K., Nam, H., & Jeon, B. (2019) · Movement Disorders · doi:10.1002/mds.27914 · Cited by 50
Kromer, R., Buhmann, C., Hidding, U., Keserü, M., Keserü, D., Hassenstein, A., & Stemplewitz, B. (2016) · PLoS ONE · doi:10.1371/journal.pone.0161136 · Cited by 47
“Second, optic neuropathy is the disease-defining factor in NTG and is suspected to play a role in PD [53,54].”
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“They stated that increased OPL Table 2 Comparison of retinal layer thickness and volumes between Parkinson and control subjects Retinal OCT parameters Unilateral Parkinson (n 28) Bilateral Parkinson (n 30) Control group (n 30) P value (UPD vs BPD) P value (UPD vs control) P value (BPD vs control) Retinal layer thickne…”
BackgroundInfluentialOphthalmic manifestations of inherited neurodegenerative disorders
Kersten, H. M., Roxburgh, R. H., & Danesh-Meyer, H. V. (2014) · Nature Reviews Neurology · doi:10.1038/nrneurol.2014.79 · Cited by 43
Bittersohl, D., Stemplewitz, B., Keserü, M., Buhmann, C., Richard, G. W., & Hassenstein, A. (2015) · Acta Ophthalmologica · doi:10.1111/aos.12757 · Cited by 42
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Turcano, P., Chen, J. J.-W., Bureau, B. L., & Savica, R. (2018) · Journal of Neurology · doi:10.1007/s00415-018-9051-0 · Cited by 41
Progressive Changes in the Retinal Structure of Patients with Parkinson’s Disease
Ma, L., Xu, L., Mao, C., Fu, Y., Ji, X., Shen, Y., Chen, J., Yang, Y., & Liu, C. (2018) · Journal of Parkinson s Disease · doi:10.3233/jpd-171184 · Cited by 40
Rojas, P., de Hoz, R., Ramirez, A. I., Ferreras, A., Salobrar‐García, E., Muñoz-Blanco, J. L., Urcelay-Segura, J. L., Salazar, J. J., & Ramirez, J. M. (2019) · Brain Sciences · doi:10.3390/brainsci9120337 · Cited by 40
Optical coherence tomography findings in Parkinson's disease
Türkoğlu, Ş. A., Umit, D., Öğün, M. N., Ulaş, F., Keleş, A., Nefise, O. Y., & Serpil, Y. (2017) · The Kaohsiung Journal of Medical Sciences · doi:10.1016/j.kjms.2017.11.006 · Cited by 36
“[7,14] investigating the relationship between IPD and RNFLT using OCT.”
MethodMultimodal retinal imaging to detect and understand Alzheimer’s and Parkinson’s disease
Moons, L., & Groef, L. D. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.07.007 · Cited by 35
Robbins, C. B., Grewal, D. S., Thompson, A. C., Soundararajan, S., Yoon, S. P., Polascik, B. W., Scott, B. L., & Fekrat, S. (2021) · Ophthalmology Retina · doi:10.1016/j.oret.2021.03.006 · Cited by 34
Rascunà, C., Cicero, C. E., Chisari, C. G., Russo, A., Giuliano, L., Castellino, N., Terravecchia, C., Grillo, M., Longo, A., Avitabile, T., et al. (2021) · Parkinsonism & Related Disorders · doi:10.1016/j.parkreldis.2021.05.031 · Cited by 34
Retinal imaging biomarkers of neurodegenerative diseases
Christinaki, E., Kulenovic, H., Hadoux, X., Baldassini, N., Eijgen, J. V., Groef, L. D., Stalmans, I., & van Wijngaarden, P. (2021) · Clinical and Experimental Optometry · doi:10.1080/08164622.2021.1984179 · Cited by 35
Retinal Degeneration: A Window to Understand the Origin and Progression of Parkinson’s Disease?
Zhang, Y., Zhang, X., Yue, Y., & Tian, T. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.799526 · Cited by 32
Retinal Findings on OCT in Systemic Conditions
Chhablani, P. P., Ambiya, V., Nair, A. G., Bondalapati, S., & Chhablani, J. K. (2017) · Seminars in Ophthalmology · doi:10.1080/08820538.2017.1332233 · Cited by 29
The role of Optical Coherence Tomography in Parkinsonism: A critical review
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Guo, B., Huang, Y., Gao, Q., & Zhou, Q. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.09.011 · Cited by 25
Stemplewitz, B., Keserü, M., Bittersohl, D., Buhmann, C., Skevas, C., Richard, G. W., & Hassenstein, A. (2015) · Acta Ophthalmologica · doi:10.1111/aos.12764 · Cited by 26
Neuroretinal Biomarkers for Schizophrenia Spectrum Disorders
Asanad, S., O’Neill, H., Addis, H., Chen, S., Jingtao, W., Goldwaser, E. L., Kochunov, P. V., Hong, L. E., & Saeedi, O. J. (2021) · Translational Vision Science & Technology · doi:10.1167/tvst.10.4.29 · Cited by 25
Retinal functional and structural changes in patients with Parkinson’s disease
Elanwar, R., Masry, H. A. E., Ibrahim, A., Hussein, M., Ibrahim, S. H., & Masoud, M. M. (2023) · BMC Neurology · doi:10.1186/s12883-023-03373-6 · Cited by 24
Optical coherence tomography neurodegenerative findings in patients with bipolar disorder
Gökçınar, N. B., Buturak, Ş. V., Özkal, F., Ozcicek, G., Yumuşak, E., & Turgal, E. (2020) · Asia-Pacific Psychiatry · doi:10.1111/appy.12394 · Cited by 21
Evaluation of retinal alterations in Parkinson disease and tremor diseases
Tuğcu, B., Melikov, A., Yıldız, G. B., Gökçal, E., Ercan, R., Uysal, Ö., & Özdemir, H. (2019) · Acta Neurologica Belgica · doi:10.1007/s13760-019-01228-x · Cited by 20
Visual hallucinations in Parkinson’s disease are associated with thinning of the inner retina
Visser, F., Apostolov, V., Vlaar, A. M. M., Twisk, J. W. R., Weinstein, H. C., & Berendse, H. W. (2020) · Scientific Reports · doi:10.1038/s41598-020-77833-1 · Cited by 18
Optical coherence tomography as a biomarker in multiple sclerosis
Fjeldstad, A. S., Carlson, N. G., & ROSE, J. W. (2012) · Expert Opinion on Medical Diagnostics · doi:10.1517/17530059.2012.719496 · Cited by 17
“One study revealed a decreased thickness of the RNFL in the temporal quadrant [56], whereas the thickness in the inferior quadrant was significantly thinner than that of controls and the temporal inferior area reported as the thinnest [57].”
BackgroundOptical coherence tomography of patients with Parkinson’s disease and progressive supranuclear palsy
Alkabie, S., Lange, A. P., Manogaran, P., Stoessl, A. J., Costello, F., & Barton, J. J. S. (2019) · Clinical Neurology and Neurosurgery · doi:10.1016/j.clineuro.2019.105635 · Cited by 18
Genetic Neuropathy Due to Impairments in Mitochondrial Dynamics
Sharma, G., Pfeffer, G., & Shutt, T. E. (2021) · Biology · doi:10.3390/biology10040268 · Cited by 18
“Notably, optic neuropathy occurs in other neurodegenerative conditions with mitochondrial transport defects such as Parkinson disease [297] and Huntington disease [298].”
BackgroundIn vivo exploration of retinal nerve fiber layer morphology in Parkinson’s disease patients
Visser, F., Vermeer, K. A., Ghafaryasl, B., Vlaar, A. M. M., Apostolov, V., Hubar, J. V. H., Weinstein, H. C., de Boer, J. F., & Berendse, H. W. (2018) · Journal of Neural Transmission · doi:10.1007/s00702-018-1872-6 · Cited by 15
Changes of Retina Are Not Involved in the Genesis of Visual Hallucinations in Parkinson’s Disease
Kopal, A., Mejzlíková, E., Preiningerova, J. L., Brebera, D., Ulmanová, O., Ehler, E., & Roth, J. (2015) · Parkinson s Disease · doi:10.1155/2015/709191 · Cited by 15
“2013 [21] 41 86 Thinning of RNFL layer in the temporal quadrant 0.”
BackgroundSekimitsu, S., Shweikh, Y., Shareef, S., Zhao, Y., Elze, T., Segrè, A. V., Wiggs, J. L., & Zebardast, N. (2023) · British Journal of Ophthalmology · doi:10.1136/bjo-2022-322762 · Cited by 14
The macular inner plexiform layer thickness as an early diagnostic indicator for Parkinson’s disease
Wang, X., Jiao, B., Jia, X., Wang, Y., Liu, H., Zhu, X., Hao, X., Zhu, Y., Xu, B., Zhang, S., et al. (2022) · npj Parkinson s Disease · doi:10.1038/s41531-022-00325-8 · Cited by 13
Optic Disc and Retinal Nerve Fibre Layer Changes in Parkinson’s Disease
Çetin, E. N., Bir, L. S., Saraç, G., Yaldızkaya, F., & Yaylalı, V. (2013) · Neuro-Ophthalmology · doi:10.3109/01658107.2012.757788 · Cited by 12
“Each patient with PD underwent neurological examination on the same day and disease severity was scored based on cognitive disturbances, activities of daily living, motor features of PD.9 They were also categorised according to existence of tremor and postural instability status.”
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Morgia, C. L., Carelli, V., & Sadun, A. A. (2021) · Handbook of clinical neurology · doi:10.1016/b978-0-12-819975-6.00020-0 · Cited by 10
Recent advances in neurology 2013–2014
Schapira, A. H. V. (2014) · European Journal of Neurology · doi:10.1111/ene.12619 · Cited by 10
Retinal Changes in Parkinson's Disease
Mailankody, P., Battu, R., Lenka, A., Shereef, P. M. M., Thennarasu, K., Yadav, R., & Pal, P. K. (2022) · Neurology India · doi:10.4103/0028-3886.349658 · Cited by 9
Eye as an object of investigation of cognitive impairment in Parkinson's disease
Litvinenko, I., Dynin, P. S., Trufanov, A. G., Gimadutdinov, R. F., & Maltsev, D. S. (2018) · S S Korsakov Journal of Neurology and Psychiatry · doi:10.17116/jnevro2018118062105 · Cited by 9
Reduction of Retinal Thickness Ipsilateral to Hippocampal Sclerosis in Epilepsy
Xiong, W., Lu, L., Chen, Q., Xiao, Y., An, D., Sander, J. W. A. S., Zhang, M., & Zhou, D. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.663559 · Cited by 8
“In PD, several studies reported intraocular asymmetry in the retinal thickness, as well as the extent of vessel changes, with more seen in the eye contralateral to the more affected body side, supporting an asymmetry of the neurodegenerative process involving the substantia nigra and the eye on the same side (18, 19);…”
ResultThe Impact of the Eye in Dementia: The Eye and its Role in Diagnosis and Follow‐up
Salobrar‐García, E., Ramirez, A. I., de Hoz, R., Rojas, P., Salazar, J. J., Rojas, B., Yubero, R., Gil, P., Triviño, A., & Ramirez, J. M. (2016) · InTech eBooks · doi:10.5772/64490 · Cited by 10
Yang, T., Xie, L.-Q., Zhang, Y., Liu, S.-M., Zeng, X., Luo, W., & Xu, G. (2023) · International Journal of Ophthalmology · doi:10.18240/ijo.2023.05.14 · Cited by 7
Wilson, D., Hallett, M., & Anderson, T. (2021) · Movement Disorders Clinical Practice · doi:10.1002/mdc3.13317 · Cited by 7
Donato, L., Scimone, C., Alibrandi, S., Vadalà, M., Castellucci, M., Bonfiglio, V. M. E., Scalinci, S. Z., Abate, G., D’Angelo, R., & Sidoti, A. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e34756 · Cited by 6
“The observed DMR profiles across genes involved in retinal degeneration ( LRRK2 ) [82], immune surveillance ( KIR2DL1 , KIR2DL3 ) [83], sphingolipid metabolism ( SPHK2 ), DNA repair ( ERCC2 ), chromatin remodeling ( MTA3 ) [84], mitochondrial gene expression ( POLRMT ) [85], structural and…”
BackgroundOcular and inflammatory markers associated with Gulf War illness symptoms
Kalahasty, K., Lee, Y., Locatelli, E. V. T., Djulbegovic, M. B., Cabrera, K., Pakravan, P., Goodman, C. S., Jensen, A., Aenlle, K. K., Klimas, N. G., et al. (2023) · Scientific Reports · doi:10.1038/s41598-023-30544-9 · Cited by 5
Neuro-ophthalmology of movement disorders
Waln, O., & Jankovic, J. J. (2018) · Expert Review of Ophthalmology · doi:10.1080/17469899.2018.1513328 · Cited by 5
Optical coherence tomography findings in chronic progressive external ophthalmoplegia
Wu, Y. F., Kang, L., Wu, H., Hou, Y., & Wang, Z.-X. (2019) · Chinese Medical Journal · doi:10.1097/cm9.0000000000000262 · Cited by 4
Suciu, V.-I., Suciu, C.-I., Nicoară, S., & Perju‐Dumbravă, L. (2022) · Journal of Personalized Medicine · doi:10.3390/jpm12010080 · Cited by 6
“The mitochondrial dysfunction in PD could lead to the axonal loss of the papillo-macular bundle [15,17,18].”
BackgroundAnimal Models and Experimental Research in Medicine
Karapehlivan, M., Gelen, V., & Kükürt, A. (2022) · IntechOpen eBooks · doi:10.5772/intechopen.100993 · Cited by 4
Stroe, A. Z., Jurja, S., Stuparu, A. F., & Axelerad, A. D. (2023) · Neurology International · doi:10.3390/neurolint15010012 · Cited by 4
Svetel, M., Maric, G. D., Bozic, M. M., Lazić, U., Milovanović, A., Jakšić, J., Petrović, I. N., Dimitrijević, A., Knežević, M., & Pekmezovic, T. D. (2025) · Biomedicines · doi:10.3390/biomedicines13051227 · Cited by 3
“Certain investigations [38,53,54] indicated a reduced RNFL thickness on the contralateral side to the more affected body side.”
Optic Disc and Retinal Architecture Changes in Patients with Spinocerebellar Ataxia Type 2
Filho, F. M. R., Jurkutė, N., de Andrade, J. B. C., Marianelli, B. F., de Lima, F. D., França, M. C., Sallum, J. M. F., Yu‐Wai‐Man, P., Barsottini, O. G. P., & Pedroso, J. L. (2023) · Movement Disorders · doi:10.1002/mds.29675 · Cited by 4
Karatzetzou, S., Parissis, D., Ioannidis, S., Afrantou, T., & Ioannidis, P. (2024) · Applied Sciences · doi:10.3390/app14062491 · Cited by 3
Metabolic Deficits in the Retina of a Familial Dysautonomia Mouse Model
Costello, S. M., Schultz, A., Smith, D. E., Horan, D., Chaverra, M., Tripet, B., George, L., Bothner, B. B., Lefcort, F. B., & Copié, V. (2024) · Metabolites · doi:10.3390/metabo14080423 · Cited by 3
Miri, S., Glazman, S., & Bodis-Wollner, I. G. (2016) · Springer eBooks · doi:10.1007/978-3-319-24085-5_6 · Cited by 3
Clinical Updates and Recent Developments in Neuro-Ophthalmology
Vuppala, A.-A. D., & Miller, N. R. (2019) · Springer eBooks · doi:10.1007/978-3-030-25389-9_8 · Cited by 3
The search for Parkinson disease biomarkers
Adams, J., & Morgia, C. L. (2018) · Neurology · doi:10.1212/wnl.0000000000006148 · Cited by 3
“These findings may point to a pathologic connection between the retina and basal ganglia in PD and are in line with previous studies reporting asymmetric retinal nerve fiber layer loss, more evident in the eye contralateral to the most affected body side.(8,9) In addition, the study used a cohort of drug-naive patient…”
ResultOCT in Parkinson’s Disease and Related Disorders
Bodis-Wollner, I. G., Miri, S., Glazman, S., Shrier, E. M., & Deeb, R. (2020) · Springer eBooks · doi:10.1007/978-3-030-26269-3_12 · Cited by 2
Dopaminergic Basis of Spatial Deficits in Early Parkinson’s Disease
Hanna‐Pladdy, B., Pahwa, R., & Lyons, K. E. (2021) · Cerebral Cortex Communications · doi:10.1093/texcom/tgab042 · Cited by 2
Neuro-Ophthalmologic Evaluation as a Biomarker for Diagnosis and Progression in Parkinson Disease
Satué, M., Polo, V., Otin, S., Larrosa, J. M., Obís, J., & García‐Martín, E. (2016) · InTech eBooks · doi:10.5772/62877 · Cited by 2
Retinal Imaging Techniques for Neurodegenerative Diseases: Parkinson's Disease and Beyond
Tang, C., Zhang, X., Miao, H., Wang, X., & Liu, J. (2025) · MedComm – Future Medicine · doi:10.1002/mef2.70034 · Cited by 1
Polekhina, N. V., Сурнина, З. В., & Zakharova, M. N. (2018) · Annals of Clinical and Experimental Neurology · doi:10.25692/acen.2018.3.9 · Cited by 1
Neurodegenerative changes of retina in Parkinson disease
Fedotova, E. Y., Полькина, Н. В., Mikhailova, E. N., & Illarioshkin, S. N. (2022) · Russian neurological Journal · doi:10.30629/2658-7947-2021-26-6-29-34 · Cited by 1
Manchanda, R., Samanta, R., Narayan, M. L., Kumar, M., Tiwari, A., Agarwal, A., Bahurupi, Y. A., Kumari, S., & Kumar, N. (2024) · Annals of Indian Academy of Neurology · doi:10.4103/aian.aian_31_24 · Cited by 1
“While the first study involving 43 PD patients and 86 HCs reported asymmetrical contralateral peripapillary RNFL thinning in PD, [11] the second study from UK involving 25 PD patients and 25 HCs reported thinning of the contralateral hemi‑retinae including macular parameters in PD patients.”
Reply to a Letter by Dr. Stefani and Colleagues on: “Auditory Dysfunction in Parkinson's Disease”
Jafari, Z., Kolb, B. E., & Mohajerani, M. H. (2020) · Movement Disorders · doi:10.1002/mds.28133 · Cited by 1
Animal Models in Neuro Ophthalmology
Normando, E. M., Brodie, J. T., & Cordeiro, M. F. (2016) · Springer eBooks · doi:10.1007/978-3-319-24085-5_13
Parkinson Hastalığı Olan Bir Olguda Optik Atrofi
Dadacı, Z., Doğanay, F., Acır, N. Ö., & Kadıyoran, C. (2019) · Selçuk Tıp Dergisi · doi:10.30733/std.2019.01058
Metadata
- Authors
- La Morgia, C., Barboni, P., Rizzo, G., Carbonelli, M., Savini, G., Scaglione, C., Capellari, S., Bonazza, S., Giannoccaro, M. P., Calandra‐Buonaura, G., Liguori, R., Cortelli, P., Martinelli, P., Baruzzi, A., & Carelli, V.
- Affiliations
- University of Bologna (IT)
- Istituto delle Scienze Neurologiche di Bologna (IT)
- Fondazione G.B. Bietti (IT)
- ORCID
- Venue
- European Journal of Neurology
- Publisher
- Wiley
- Published
- 2012-03-21
- Volume
- 20
- Issue
- 1
- Pages
- 198-201
- ISSN
- 1351-5101 (ISSN-L)
- 1468-1331
- OpenAlex
- W2152613502
- Cited by
- 110
- References
- 18
- Citations by year
- 2026: 1 · 2025: 6 · 2024: 4 · 2023: 7 · 2022: 9 · 2021: 11 · 2020: 13 · 2019: 12 · 2018: 9 · 2017: 10 · 2016: 10 · 2015: 4 · 2014: 5 · 2013: 6 · 2012: 3
- FWCI
- 3.75
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- European Journal of Neurology (publishedVersion)
- PubMed (publishedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Topics
- Health Sciences › Medicine › Clinical Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Ophthalmology › Glaucoma and retinal disorders
- Health Sciences › Medicine › Ophthalmology › Drug-Induced Ocular Toxicity
- Keywords
- Parkinson's disease, retinal nerve fiber layer thickness, temporal quadrant, mitochondrial optic neuropathy, mitochondrial disease, optic nerve involvement, retinal abnormalities, fellow eye
- MeSH terms
- Leucine-Rich Repeat Serine-Threonine Protein Kinase-2, Adult, Aged, Aged, 80 and over, Female, Humans, Male, Middle Aged, Mutation, Nerve Fibers, Optic Nerve, Optic Nerve Diseases, Parkinson Disease, Retina, Case-Control Studies, Protein Serine-Threonine Kinases, Tomography, Optical Coherence
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