Changes in corneal nerves fibers in the early stages of Parkinson’s disease according to in vivo confocal microscopy (preliminary report)

Avetisov S.E.; Karabanov A.V.; Surnina Z.V.; Gamidov A.A.

doi:https://doi.org/10.17116/oftalma2020136052191

Avetisov S.E.

Krasnov Research Institute of Eye Disease;
I.M. Sechenov First Moscow State Medical University (Sechenov University)

ORCID: 0000-0001-7115-4275

Karabanov A.V.

Research Center of Neurology

Surnina Z.V.

Krasnov Research Institute of Eye Diseases

ORCID: 0000-0001-5692-1800

Gamidov A.A.

Krasnov Research Institute of Eye Diseases

ORCID: 0000-0002-9192-449X

Changes in corneal nerves fibers in the early stages of Parkinson’s disease according to in vivo confocal microscopy (preliminary report)

Authors:

Avetisov S.E., Karabanov A.V., Surnina Z.V., Gamidov A.A.

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Journal: Russian Annals of Ophthalmology. 2020;136(5): 191‑196

DOI: 10.17116/oftalma2020136052191

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To cite this article:

Avetisov SE, Karabanov AV, Surnina ZV, Gamidov AA. Changes in corneal nerves fibers in the early stages of Parkinson’s disease according to in vivo confocal microscopy (preliminary report). Russian Annals of Ophthalmology. 2020;136(5):191‑196. (In Russ.)
https://doi.org/10.17116/oftalma2020136052191

Подписка 2026 Вестник офтальмологии (Russian Annals of Ophthalmology)

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PURPOSE

To analyze the changes in the course and structure of corneal nerve fibers in the early stages of Parkinson’s disease based on an objective algorithm of in vivo corneal confocal microscopy (CCM).

MATERIAL AND METHODS

The study was conducted on a group of 16 patients aged 39 to 66 years with verified diagnosis of PD. In addition to standard neurological and ophthalmological examinations, all patients underwent IVCCM on a Heidelberg Retinal Tomograph device with special Rostock Cornea Module (HRT3 RCM), followed by processing of the obtained images using a uniquely designed analysis algorithm.

RESULTS

A significant decrease in the directional anisotropy coefficient and an increase in the directional symmetry coefficient of the nerve fibers of the cornea were established (average values 3.15±1.08 and 0.92±0.04, respectively); in healthy individuals of the identical age range these indicators are 3.5±0.85 and 0.86±0.11, respectively. In addition, qualitative structural changes were noted, which consisted of an increase in the number of branches from the main nerve trunks, an increase in the tortuosity of CNF, multidirectionality, and “beaded” shape. In 9 cases, the presence of macrophages was revealed — dendritic Langerhans cells, which is an indirect sign of the inflammatory process.

CONCLUSION

The preliminary nature of the results obtained in this study and the need for further research in this area are related, on the one hand, to a small sample of observations and, on the other hand, to the criterion used to assess the status of CNF based on a comparative analysis with conditionally normal indicators. In the future, in order to solve the problem of the uniqueness of changes in CNF and the possibility of using these changes as a marker for PD progression, longitudinal studies are required to reveal the presence or absence of a correlation between the stage of the disease, the results of known monitoring methods (e.g. electromyography) and quantitative indicators of the status of CNF.

Keywords:

Parkinson’s disease

corneal nerve fibers

in vivo corneal confocal microscopy

Authors:

Avetisov S.E.

Krasnov Research Institute of Eye Disease;
I.M. Sechenov First Moscow State Medical University (Sechenov University)

ORCID: 0000-0001-7115-4275

Karabanov A.V.

Research Center of Neurology

Surnina Z.V.

Krasnov Research Institute of Eye Diseases

ORCID: 0000-0001-5692-1800

Gamidov A.A.

Krasnov Research Institute of Eye Diseases

ORCID: 0000-0002-9192-449X

Received:

24.04.2020

Accepted:

19.05.2020

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References:

Eduardo M, Davis B, Groef L, et al. The retina as an early biomarker of neurodegeneration in a rotenone-induced model of Parkinson’s disease: evidence for a neuroprotective effect of rosiglitazone in the eye and brain. Acta Neuropathologica Communications. 2016;4:86. https://doi.org/10.1186/s40478-016-0346-z
Grayson M. Parkinson’s disease. Nature. 2016;538:1. https://doi.org/10.1038/538s1a
Bogdanov RR, Bogdanov AR, Kotov SV. Management tactics for patients with initial manifestations of Parkinson’s disease. Nevrologia. 2012;5(73):15-21. (In Russ.).
Wolters E, Francot C, Bergmans P, Winogrodzka A, Booy J, Berendse H, et al. Preclinical (premotor) Parkinson’s disease. J Neurol. 2000;247(2):103-109.
Braak H, Del Tredici K, Rueb U, de Vos R, et. al. Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging. 2003;24:197-211. https://doi.org/10.1016/s0197-4580(02)00065-9
Hawkes CH. The prodromal phase of sporadic Parkinson’s disease: does it exist and if so how long is it? Mov Disord. 2008;23:1799-1807. https://doi.org/10.1002/mds.22242
Wolters E. Variability in the clinical expression of Parkinson’s disease. J Neurol Sci. 2008;266:197-203. https://doi.org/10.1016/j.jns.2007.08.016
Chaudhuri K, Schapira A. Non-motor symptoms of Parkinson’s disease: dopaminergic pathophysiology and treatment. Lancet Neurol. 2009;8:464-474. https://doi.org/10.1016/s1474-4422 (09)70068-7
Bogdanov RR, Kotov SV, Kunitsyna AN, Turbina LG. Drug correction of motor manifestations of the advanced stages of Parkinson’s disease. Zurnal nevrologii i psihiatrii. 2010;11:11-21. (In Russ.).
Levin OS, Fedorova NV. Bolezn’ Parkinsona. M. 2006. (In Russ.).
Gaenslen A. Early diagnosis of Parkinson’s disease. Int Rev Neurobiol. 2010; 90:81-92.
Brooks DJ. Morphological and functional imaging studies on the diagnosis and progression of Parkinson’s disease. J Neurol. 2000;247(2):11-18. https://doi.org/10.1007/pl00007755
Nuytemans K, Theuns J, Cruts M, Broeckhoven C Van, et al. Genetic etiology of Parkinson disease associated with mutations in the SNCA, PARK2, PINK1, PARK7, and LRRK2 genes: a mutation update. Hum Mutat. 2010; 31(7):763-780. https://doi.org/10.1002/humu.21277
Marder KS, Tang M, Mejia-Santana H, Rosado L, et. al. Predictors of parkin mutations in early-onset Parkinson disease: the consortium on risk for early-onset Parkinson disease study. Arch Neurol. 2010;67(6):731-738. https://doi.org/10.1001/archneurol.2010.95
Rachakonda V, Pan T, Le W, et. al. Biomarkers of neurodegenerative disorders: how good are they? Cell Res. 2004;14(5):347-358. https://doi.org/10.1038/sj.cr.7290235
Robinson PA. Understanding the molecular basis of Parkinson’s disease, identification of biomarkers and routes to therapy. Expert Rev Proteomics. 2010;7(4):565-578. https://doi.org/10.1586/epr.10.40
Illarioshkin SN, Levin OS, Fedotova EYu, Kolokolov OV. Parkinsonism i chernaya substanciya. Izdatelstvo: Atmosfera; 2019. (In Russ.).
Katunina EA, Titova NV, Avakyan GN. Diagnosis methods for early Parkinson’s disease. Zurnal nevrologii i psihiatrii. 2010;110(12):112-118. (In Russ.).
Ikeda K, Kawase Y, Hasegawa K, Kawashima N, Horiuchi E, et al. Olfactory dysfunction in Parkinson’s disease: Benefits of quantitative odorant examination. Int J Gen Med. 2010;3:181-185. https://doi.org/10.2147/ijgm.s12048
Chesnokova NB, Pavlenko TA, Ugryumov MV. Pathology of the organ of vision as one of the manifestations of Parkinson’s disease. Zurnal nevrologii i psihiatrii im. S.S. Korsakova. 2017;9:124-131. (In Russ.). https://doi.org/10.17116/nevro201711791124-131
Turbina LG, Bogdanov RR, Ratmanova PO, Brinskih AM, vina EI, et al. Saccadic eye movements of patients with initial manifestations of Parkinson’s disease and the dynamics of their parameters during treatment with pyribedil. Almanah klinicheskoy medicini. MONIKI. 2005;8(3):119-124. (In Russ.).
Chambers JM. Response times for visually guided saccades in persons with Parkinson’s disease: a meta-analytic review. Neuropsychologia. 2010;48(4): 887-899. https://doi.org/10.1016/j.neuropsychologia.2009.11.006
Anang J, Gagnon J, Bertrand J. Predictors of dementia in Parkinson disease: A prospective cohort study. Neurology. 2014;83:1253-1260. https://doi.org/10.1212/wnl.0000000000001408
Armstrong RA. Visual Symptoms in Parkinson’s Disease. Research Article. Folia Neuropathol. 2007;45(3):108-114. https://doi.org/10.4061/2011/908306
Vaisman L, Zariffa J, Vaisman L. Application of singular spectrum-based change-point analysis to EMG-onset detection. J Electromyogr Kinesiol. 2010;20(4):750-760. https://doi.org/10.1016/j.jelekin.2010.02.010
Garcia-Martin E, Satue M, Fuertes I, et al. Ability and reproducibility of Fournier-domain optical coherence tomography to detect retinal nerve fiber layer atrophy in Parkinson’s disease. Ophthalmology. 2012;119(10):2157-2161. https://doi.org/10.1016/j.ophtha.2012.05.003
Stergiou V, Fotiou D, Tsiptsios D. Pupillometric findings in patients with Parkinson’s disease and cognitive disorder. Int J Psychophysiol. 2009;72(2):97-101. https://doi.org/10.1016/j.ijpsycho.2008.10.010
Demirci S, Gunes A, Koyuncuoglu H, Tok L, et. al. Evaluation of corneal parameters in patients with Parkinson’s disease. Neurol Sci. 2016;37(8):1247-1252. https://doi.org/10.1007/s10072-016-2574-1
Reddy V, Patel S, Hodge D, Leavitt J. Corneal Sensitivity, Blink Rate, and Corneal Nerve Density in Progressive Supranuclear Palsy and Parkinson Disease. CLINICAL SCIENCE. Cornea. 2013;32(5):631-635. https://doi.org/10.1097/ico.0b013e3182574ade
Ponirakis G, Hamad H Al, Sankaranarayanan A, et al. Association of corneal nerve ﬁber measures with cognitive function in dementia. Annals of Clinical and Translational Neurology. 2019;6(4):689-697. https://doi.org/10.1002/acn3.746
Avetisov SE, Novikov IA, Mahotin SS, Surnina ZV. Calculation of the coefficients of anisotropy and symmetry of the orientation of the corneal nerves based on the automated recognition of digital confocal images. Medicinskaya technika. 2015;3:23-25. (In Russ.).
Örnek N, Dağ E, Örnek K, et al. Corneal sensitivity and tear function in neurodegenerative diseases. Curr Eye Res. 2015;40(4):423-428. https://doi.org/10.3109/02713683.2014.930154
Avetisov SE, Surnina ZV, Novikov IA, Chernenkova NA, Turina AA. The effect of the tear film on the results of a direct assessment of the sensitivity of the cornea. Vestnik oftal’mologii. 2020;136(2):81-85. (In Russ.). https://doi.org/10.17116/oftalma202013602181
Dipika V, Jie Z, Charles NJ. In vivo confocal microscopy of the inflamed anterior segment: A review of clinical and research applications. Clinical & Experimental Ophthalmology. 2019;47(3):334-345. https://doi.org/10.1111/ceo.13512