Abnormalities of the oculomotor function in type 1 diabetes and diabetic neuropathy.


Journal

Acta diabetologica
ISSN: 1432-5233
Titre abrégé: Acta Diabetol
Pays: Germany
ID NLM: 9200299

Informations de publication

Date de publication:
Sep 2022
Historique:
received: 29 03 2022
accepted: 23 05 2022
pubmed: 22 6 2022
medline: 30 7 2022
entrez: 21 6 2022
Statut: ppublish

Résumé

Abnormalities in the oculomotor system may represent an early sign of diabetic neuropathy and are currently poorly studied. We designed an eye-tracking-based test to evaluate oculomotor function in patients with type 1 diabetes. We used the SRLab-Tobii TX300 Eye tracker®, an eye-tracking device, coupled with software that we developed to test abnormalities in the oculomotor system. The software consists of a series of eye-tracking tasks divided into 4 classes of parameters (Resistance, Wideness, Pursuit and Velocity) to evaluate both smooth and saccadic movement in different directions. We analyzed the oculomotor system in 34 healthy volunteers and in 34 patients with long-standing type 1 diabetes. Among the 474 parameters analyzed with the eye-tracking-based system, 11% were significantly altered in patients with type 1 diabetes (p < 0.05), with a higher proportion of abnormalities observed in the Wideness (24%) and Resistance (10%) parameters. Patients with type 1 diabetes without diabetic neuropathy showed more frequently anomalous measurements in the Resistance class (p = 0.02). The classes of Velocity and Pursuit were less frequently altered in patients with type 1 diabetes as compared to healthy subjects, with anomalous measurements mainly observed in patients with diabetic neuropathy. Abnormalities in oculomotor system function can be detected in patients with type 1 diabetes using a novel eye-tracking-based test. A larger cohort study may further determine thresholds of normality and validate whether eye-tracking can be used to non-invasively characterize early signs of diabetic neuropathy. NCT04608890.

Identifiants

pubmed: 35729357
doi: 10.1007/s00592-022-01911-1
pii: 10.1007/s00592-022-01911-1
pmc: PMC9329167
doi:

Banques de données

ClinicalTrials.gov
['NCT04608890']

Types de publication

Clinical Study Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1157-1167

Subventions

Organisme : European Foundation for the Study of Diabetes
ID : EFSD/JDRF/Lilly Programme on Type 1 Diabetes Research 2019
Organisme : Ministero della Salute
ID : RF-2016-02362512

Informations de copyright

© 2022. The Author(s).

Références

Mizokami-Stout KR, Li Z, Foster NC et al (2020) The contemporary prevalence of diabetic neuropathy in type 1 diabetes: findings from the T1D exchange. Diabetes Care 43:806–812
pubmed: 32029635 pmcid: 7085805 doi: 10.2337/dc19-1583
Perkins BA (2020) Rethinking neuropathy in type 1 diabetes: had we lost sight of what matters most? Diabetes Care 43:695–697
pubmed: 32198282 doi: 10.2337/dci19-0076
Vinik AI (2016) Clinical practice: diabetic sensory and motor neuropathy. N Engl J Med 374:1455–1464
pubmed: 27074068 doi: 10.1056/NEJMcp1503948
Feldman EL, Callaghan BC, Pop-Busui R et al (2019) Diabetic neuropathy. Nat Rev Dis Primers 5:41
pubmed: 31197153 doi: 10.1038/s41572-019-0092-1
Callaghan BC, Cheng HT, Stables CL, Smith AL, Feldman EL (2012) Diabetic neuropathy: clinical manifestations and current treatments. Lancet Neurol 11:521–534
pubmed: 22608666 pmcid: 4254767 doi: 10.1016/S1474-4422(12)70065-0
Selvarajah D, Kar D, Khunti K et al (2019) Diabetic peripheral neuropathy: advances in diagnosis and strategies for screening and early intervention. Lancet Diabetes Endocrinol 7:938–948
pubmed: 31624024 doi: 10.1016/S2213-8587(19)30081-6
Jaiswal M, Divers J, Dabelea D et al (2017) Prevalence of and risk factors for diabetic peripheral neuropathy in youth with type 1 and type 2 diabetes: SEARCH for diabetes in youth study. Diabetes Care 40:1226–1232
pubmed: 28674076 pmcid: 5566278 doi: 10.2337/dc17-0179
Tesfaye S, Sloan G (2020) Diabetic polyneuropathy: advances in diagnosis and intervention strategies. Eur Endocrinol 16:15–20
pubmed: 32595764 pmcid: 7308107 doi: 10.17925/EE.2020.16.1.15
Vinik AI, Nevoret ML, Casellini C, Parson H (2013) Diabetic neuropathy. Endocrinol Metab Clin North Am 42:747–787
pubmed: 24286949 doi: 10.1016/j.ecl.2013.06.001
Vinik AI, Holland MT, Le Beau JM, Liuzzi FJ, Stansberry KB, Colen LB (1992) Diabetic neuropathies. Diabetes Care 15:1926–1975
pubmed: 1464246 doi: 10.2337/diacare.15.12.1926
Veresiu AI, Bondor CI, Florea B, Vinik EJ, Vinik AI, Gavan NA (2015) Detection of undisclosed neuropathy and assessment of its impact on quality of life: a survey in 25,000 Romanian patients with diabetes. J Diabetes Complicat 29:644–649
doi: 10.1016/j.jdiacomp.2015.04.001
Pop-Busui R, Boulton AJ, Feldman EL et al (2017) Diabetic neuropathy: a position statement by the American diabetes association. Diabetes Care 40:136–154
pubmed: 27999003 doi: 10.2337/dc16-2042
Louraki M, Karayianni C, Kanaka-Gantenbein C, Katsalouli M, Karavanaki K (2012) Peripheral neuropathy in children with type 1 diabetes. Diabetes Metab 38:281–289
pubmed: 22503144 doi: 10.1016/j.diabet.2012.02.006
Breiner A, Lovblom LE, Perkins BA, Bril V (2014) Does the prevailing hypothesis that small-fiber dysfunction precedes large-fiber dysfunction apply to type 1 diabetic patients? Diabetes Care 37:1418–1424
pubmed: 24574353 doi: 10.2337/dc13-2005
Buttner-Ennever JA (2007) Anatomy of the oculomotor system. Dev Ophthalmol 40:1–14
pubmed: 17314476 doi: 10.1159/000100345
Virtaniemi J, Laakso M, Nuutinen J, Karjalainen S, Vartiainen E (1993) Voluntary eye movement tests in patients with insulin-dependent diabetes mellitus. Acta Otolaryngol 113:123–127
pubmed: 8475725 doi: 10.3109/00016489309135779
Gawron W, Pospiech L, Orendorz-Fraczkowska K, Noczynska A (2002) Are there any disturbances in vestibular organ of children and young adults with Type I diabetes? Diabetologia 45:728–734
pubmed: 12107754 doi: 10.1007/s00125-002-0813-x
Bueno APA, Sato JR, Hornberger M (2019) Eye tracking: the overlooked method to measure cognition in neurodegeneration? Neuropsychologia 133:107191
pubmed: 31521634 doi: 10.1016/j.neuropsychologia.2019.107191
Tao L, Wang Q, Liu D, Wang J, Zhu Z, Feng L (2020) Eye tracking metrics to screen and assess cognitive impairment in patients with neurological disorders. Neurol Sci 41:1697–1704
pubmed: 32125540 doi: 10.1007/s10072-020-04310-y
Garcia-Diaz A, Leboran V, Fdez-Vidal XR, Pardo XM (2012) On the relationship between optical variability, visual saliency, and eye fixations: a computational approach. J Vis 12:17
pubmed: 22693335 doi: 10.1167/12.6.17
Tesfaye S, Boulton AJ, Dyck PJ et al (2010) Diabetic neuropathies: update on definitions, diagnostic criteria, estimation of severity, and treatments. Diabetes Care 33:2285–2293
pubmed: 20876709 pmcid: 2945176 doi: 10.2337/dc10-1303
Gibaldi A, Vanegas M, Bex PJ, Maiello G (2017) Evaluation of the tobii eyeX eye tracking controller and matlab toolkit for research. Behav Res Methods 49:923–946
pubmed: 27401169 doi: 10.3758/s13428-016-0762-9
Bonhof GJ, Herder C, Strom A, Papanas N, Roden M, Ziegler D (2019) Emerging biomarkers, tools, and treatments for diabetic polyneuropathy. Endocr Rev 40:153–192
pubmed: 30256929 doi: 10.1210/er.2018-00107
Callaghan BC, Gallagher G, Fridman V, Feldman EL (2020) Diabetic neuropathy: what does the future hold? Diabetologia 63:891–897
pubmed: 31974731 pmcid: 7150623 doi: 10.1007/s00125-020-05085-9
Dewanjee S, Das S, Das AK et al (2018) Molecular mechanism of diabetic neuropathy and its pharmacotherapeutic targets. Eur J Pharmacol 833:472–523
pubmed: 29966615 doi: 10.1016/j.ejphar.2018.06.034
Dyck PJ, Albers JW, Andersen H et al (2011) Diabetic polyneuropathies: update on research definition, diagnostic criteria and estimation of severity. Diabetes Metab Res Rev 27:620–628
pubmed: 21695763 doi: 10.1002/dmrr.1226
Del Carro U, Fiorina P, Amadio S et al (2007) Evaluation of polyneuropathy markers in type 1 diabetic kidney transplant patients and effects of islet transplantation: neurophysiological and skin biopsy longitudinal analysis. Diabetes Care 30:3063–3069
pubmed: 17804685 doi: 10.2337/dc07-0206
Lauria G, Devigili G (2007) Skin biopsy as a diagnostic tool in peripheral neuropathy. Nat Clin Pract Neurol 3:546–557
pubmed: 17914343 doi: 10.1038/ncpneuro0630
Dyck PJ, Argyros B, Russell JW et al (2014) Multicenter trial of the proficiency of smart quantitative sensation tests. Muscle Nerve 49:645–653
pubmed: 23929701 pmcid: 3966980 doi: 10.1002/mus.23982
Malik RA (2020) Diabetic neuropathy: a focus on small fibres. Diabetes Metab Res Rev 36(Suppl 1):e3255
pubmed: 31828951
Sveen KA, Karime B, Jorum E et al (2013) Small- and large-fiber neuropathy after 40 years of type 1 diabetes: associations with glycemic control and advanced protein glycation: the Oslo Study. Diabetes Care 36:3712–3717
pubmed: 24026557 pmcid: 3816884 doi: 10.2337/dc13-0788
Zhang X, Fang C, Li X et al (2017) Clinical characteristics and risk factors of diabetic peripheral neuropathy of type 1 diabetes mellitus patients. Diabetes Res Clin Pract 129:97–104
pubmed: 28521198 doi: 10.1016/j.diabres.2017.04.016
D’Addio F, La Rosa S, Maestroni A et al (2015) Circulating IGF-I and IGFBP3 levels control human colonic stem cell function and are disrupted in diabetic enteropathy. Cell Stem Cell 17:486–498
pubmed: 26431183 pmcid: 4826279 doi: 10.1016/j.stem.2015.07.010
D’Addio F, Trevisani A, Ben Nasr M et al (2014) Harnessing the immunological properties of stem cells as a therapeutic option for diabetic nephropathy. Acta Diabetol 51:897–904
pubmed: 24894496 doi: 10.1007/s00592-014-0603-1
Tonneijck L, Muskiet MH, Smits MM et al (2017) Glomerular hyperfiltration in diabetes: mechanisms, clinical significance, and treatment. J Am Soc Nephrol 28:1023–1039
pubmed: 28143897 pmcid: 5373460 doi: 10.1681/ASN.2016060666
Rojas DR, Kuner R, Agarwal N (2019) Metabolomic signature of type 1 diabetes-induced sensory loss and nerve damage in diabetic neuropathy. J Mol Med (Berl) 97:845–854
doi: 10.1007/s00109-019-01781-1
Venturini M, Fiorina P, Maffi P et al (2006) Early increase of retinal arterial and venous blood flow velocities at color Doppler imaging in brittle type 1 diabetes after islet transplant alone. Transplantation 81:1274–1277
pubmed: 16699454 doi: 10.1097/01.tp.0000208631.63235.6a
Grillini A, Renken RJ, Vrijling ACL, Heutink J, Cornelissen FW (2020) Eye movement evaluation in multiple sclerosis and Parkinson’s disease using a standardized oculomotor and neuro-ophthalmic disorder assessment (SONDA). Front Neurol 11:971
pubmed: 33013643 pmcid: 7506055 doi: 10.3389/fneur.2020.00971
Soans RS, Grillini A, Saxena R, Renken RJ, Gandhi TK, Cornelissen FW (2021) Eye-movement-based assessment of the perceptual consequences of glaucomatous and neuro-ophthalmological visual field defects. Transl Vis Sci Technol 10:1
pubmed: 34003886 pmcid: 7873497 doi: 10.1167/tvst.10.2.1
de Boer C, van der Steen J, Mattace-Raso F, Boon AJ, Pel JJ (2016) The effect of neurodegeneration on visuomotor behavior in Alzheimer’s disease and Parkinson’s disease. Mot Control 20:1–20
doi: 10.1123/mc.2014-0015
D’Addio F, Maffi P, Vezzulli P et al (2014) Islet transplantation stabilizes hemostatic abnormalities and cerebral metabolism in individuals with type 1 diabetes. Diabetes Care 37:267–276
pubmed: 24026546 doi: 10.2337/dc13-1663
Avendano-Valencia LD, Yderstraede KB, Nadimi ES, Blanes-Vidal V (2021) Video-based eye tracking performance for computer-assisted diagnostic support of diabetic neuropathy. Artif Intell Med 114:102050
pubmed: 33875161 doi: 10.1016/j.artmed.2021.102050

Auteurs

Francesca D'Addio (F)

International Center for T1D, Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, DIBIC, Università di Milano, Milan, Italy.

Ida Pastore (I)

Division of Endocrinology, ASST Fatebenefratelli-Sacco, Milan, Italy.

Cristian Loretelli (C)

International Center for T1D, Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, DIBIC, Università di Milano, Milan, Italy.

Alessandro Valderrama-Vasquez (A)

Nephrology Division, Boston Children's Hospital and Transplantation Research Center, Brigham and Women's Hospital, Harvard Medical School, 300 Longwood Ave., Boston, MA, 02115, USA.

Vera Usuelli (V)

International Center for T1D, Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, DIBIC, Università di Milano, Milan, Italy.

Emma Assi (E)

International Center for T1D, Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, DIBIC, Università di Milano, Milan, Italy.

Chiara Mameli (C)

Department of Pediatrics, Buzzi Children's Hospital, Milan, Italy.

Maddalena Macedoni (M)

Department of Pediatrics, Buzzi Children's Hospital, Milan, Italy.

Anna Maestroni (A)

International Center for T1D, Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, DIBIC, Università di Milano, Milan, Italy.

Antonio Rossi (A)

Division of Endocrinology, ASST Fatebenefratelli-Sacco, Milan, Italy.

Maria Elena Lunati (ME)

Division of Endocrinology, ASST Fatebenefratelli-Sacco, Milan, Italy.

Paola Silvia Morpurgo (PS)

Division of Endocrinology, ASST Fatebenefratelli-Sacco, Milan, Italy.

Alessandra Gandolfi (A)

Division of Endocrinology, ASST Fatebenefratelli-Sacco, Milan, Italy.

Laura Montefusco (L)

Division of Endocrinology, ASST Fatebenefratelli-Sacco, Milan, Italy.

Andrea Mario Bolla (AM)

Division of Endocrinology, ASST Fatebenefratelli-Sacco, Milan, Italy.

Moufida Ben Nasr (M)

International Center for T1D, Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, DIBIC, Università di Milano, Milan, Italy.
Nephrology Division, Boston Children's Hospital and Transplantation Research Center, Brigham and Women's Hospital, Harvard Medical School, 300 Longwood Ave., Boston, MA, 02115, USA.

Stefania Di Maggio (S)

International Center for T1D, Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, DIBIC, Università di Milano, Milan, Italy.

Lisa Melzi (L)

Neuro-Ophthalmology Center and Ocular Electrophysiology Laboratory, IRCCS Istituto Auxologico Italiano, Capitanio Hospital, Milan, Italy.

Giovanni Staurenghi (G)

Clinica Oculistica, ASST Fatebenefratelli-Sacco, Università di Milano, Milan, Italy.

Antonio Secchi (A)

Transplant Medicine, IRCCS Ospedale San Raffaele, Milan, Italy.

Stefania Bianchi Marzoli (S)

Neuro-Ophthalmology Center and Ocular Electrophysiology Laboratory, IRCCS Istituto Auxologico Italiano, Capitanio Hospital, Milan, Italy.

Gianvincenzo Zuccotti (G)

Pediatric Clinical Research Center Romeo Ed Enrica Invernizzi, DIBIC, Università di Milano and Department of Pediatrics, Buzzi Children's Hospital, Milan, Italy.

Paolo Fiorina (P)

International Center for T1D, Pediatric Clinical Research Center Romeo ed Enrica Invernizzi, DIBIC, Università di Milano, Milan, Italy. paolo.fiorina@childrens.harvard.edu.
Division of Endocrinology, ASST Fatebenefratelli-Sacco, Milan, Italy. paolo.fiorina@childrens.harvard.edu.
Nephrology Division, Boston Children's Hospital and Transplantation Research Center, Brigham and Women's Hospital, Harvard Medical School, 300 Longwood Ave., Boston, MA, 02115, USA. paolo.fiorina@childrens.harvard.edu.

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