Generic placeholder image

Current Diabetes Reviews

Editor-in-Chief

ISSN (Print): 1573-3998
ISSN (Online): 1875-6417

Research Article

Cognitive Performance and Diabetic Retinopathy: What Your Eyes Can Reveal About Your Brain

Author(s): Ana Cristina Ravazzani de Almeida Faria, Joceline Franco Dall'Agnol, Aline Maciel Gouveia, Clara Inácio De Paiva, Victoria Chechetto Segalla, Fernando Eiji Ogata and Cristina Pellegrino Baena*

Volume 19, Issue 9, 2023

Published on: 18 October, 2022

Article ID: e050822207323 Pages: 9

DOI: 10.2174/1573399819666220805154638

open access plus

Abstract

Background: Diabetic retinopathy (DR) is a chronic diabetes complication. People with Type 2 Diabetes Mellitus (T2DM) have two times the risk for dementia, suggesting it is a new chronic diabetes complication.

Objective: Evaluate the association of DR with cognitive performance in a T2DM population.

Methods: Cross-sectional study with 400 T2DM adults from whom socio-demographic, clinical, laboratory data were collected, and screening test for depression symptoms (Patient Health Questionaire- 9 (PHQ-9)), Mini-Mental State Examination (MMSE), Semantic Verbal Fluency Test, Trail Making Test A and B, Word Memory test were performed. All cognitive test scores were converted into Global Cognition z-Score (GCS(z)). The association between GCS(z) < 0 with DR was performed using a multivariate binary logistic regression model adjusted for age ≥ 65 years, school years ≤ 6 years, DM duration ≥ 10 years, depression symptoms score > 9 at PHQ-9, arterial hypertension, physical activity, diabetic retinopathy, macular edema, and cardiovascular disease.

Results: After exclusions, the 251 eligible patients were 56.6% female, with a mean age of 61.1 (±9.8) years, DM duration of 12.6 (±8.9) years, and 7.6 (±4.2) years of school education. DR prevalence was 46.5%. Multivariate Logistic Regression Model showed an association between DR and GCS(z) < 0, with odds ratio (CI95%) of 2.50 (1.18-5.34), adjusted for age, low education level, arterial hypertension and depression symptoms (OD and CI95% respectively: 5.46(2.42-12.34); 12.19 (5.62-26.46); 2.55 (0.88-7.39); 3.53 (1.55-8.07)).

Conclusion: In this T2DM population, having DR increased the chance for worse cognitive performance even when adjusted for age, low education level, presence of arterial hypertension, and depression symptoms.

Keywords: Diabetic retinopathy, cognitive dysfunction, type 2 diabetes mellitus, risk factors, dementia, cognitive decline.

[1]
Prince MJ, Wimo A, Guerchet MM, Ali GC, Wu Y-T, Prina M. World Alzheimer Report 2015 - The Global Impact of Dementia: An analysis of prevalence, incidence, cost and trends. London: Alzheimer's Disease International 2015.
[2]
Vos T, Lim SS, Abbafati C, et al. Global burden of 369 diseases and injuries in 204 countries and territories, 1990-2019: A systematic analysis for the Global Burden of Disease Study 2019. Lancet 2020; 396(10258): 1204-22.
[http://dx.doi.org/10.1016/S0140-6736(20)30925-9] [PMID: 33069326]
[3]
nternational Diabetes Federation. IDF Diabetes Atlas 9th ed. 2019. Available from: https://www.diabetesatlas.org
[4]
Yau JWY, Rogers SL, Kawasaki R, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 2012; 35(3): 556-64.
[http://dx.doi.org/10.2337/dc11-1909] [PMID: 22301125]
[5]
Ott A, Stolk RP, van Harskamp F, Pols HAP, Hofman A, Breteler MMB. Diabetes mellitus and the risk of dementia: The Rotterdam Study. Neurology 1999; 53(9): 1937-42.
[http://dx.doi.org/10.1212/WNL.53.9.1937] [PMID: 10599761]
[6]
Peila R, Rodriguez BL, Launer LJ. Type 2 diabetes, APOE gene, and the risk for dementia and related pathologies: The Honolulu-Asia Aging Study. Diabetes 2002; 51(4): 1256-62.
[http://dx.doi.org/10.2337/diabetes.51.4.1256] [PMID: 11916953]
[7]
Rawlings AM, Sharrett AR, Schneider ALC, et al. Diabetes in midlife and cognitive change over 20 years: A cohort study. Ann Intern Med 2014; 161(11): 785-93.
[http://dx.doi.org/10.7326/M14-0737] [PMID: 25437406]
[8]
Roberts RO, Knopman DS, Geda YE, et al. Association of diabetes with amnestic and nonamnestic mild cognitive impairment. Alzheimers Dement 2014; 10(1): 18-26.
[http://dx.doi.org/10.1016/j.jalz.2013.01.001] [PMID: 23562428]
[9]
Barnes DE, Yaffe K. The projected effect of risk factor reduction on Alzheimer’s disease prevalence. Lancet Neurol 2011; 10(9): 819-28.
[http://dx.doi.org/10.1016/S1474-4422(11)70072-2] [PMID: 21775213]
[10]
Munshi MN. Cognitive dysfunction in older adults with diabetes: What a clinician needs to know. Diabetes Care 2017; 40(4): 461-7.
[http://dx.doi.org/10.2337/dc16-1229] [PMID: 28325796]
[11]
Cukierman T, Gerstein HC, Williamson JD. Cognitive decline and dementia in diabetes-systematic overview of prospective observational studies. Diabetologia 2005; 48(12): 2460-9.
[http://dx.doi.org/10.1007/s00125-005-0023-4] [PMID: 16283246]
[12]
Zhang J, Chen C, Hua S, et al. An updated meta-analysis of cohort studies: Diabetes and risk of Alzheimer’s disease. Diabetes Res Clin Pract 2017; 124: 41-7.
[http://dx.doi.org/10.1016/j.diabres.2016.10.024] [PMID: 28088029]
[13]
Gudala K, Bansal D, Schifano F, Bhansali A. Diabetes mellitus and risk of dementia: A meta-analysis of prospective observational studies. J Diabetes Investig 2013; 4(6): 640-50.
[http://dx.doi.org/10.1111/jdi.12087] [PMID: 24843720]
[14]
Biessels GJ, Staekenborg S, Brunner E, Brayne C, Scheltens P. Risk of dementia in diabetes mellitus: A systematic review. Lancet Neurol 2006; 5(1): 64-74.
[http://dx.doi.org/10.1016/S1474-4422(05)70284-2] [PMID: 16361024]
[15]
Simó R, Ciudin A, Simó-Servat O, Hernández C. Cognitive impairment and dementia: A new emerging complication of type 2 diabetes-The diabetologist’s perspective. Acta Diabetol 2017; 54(5): 417-24.
[http://dx.doi.org/10.1007/s00592-017-0970-5] [PMID: 28210868]
[16]
Ferreira ST, Clarke JR, Bomfim TR, De Felice FG. Inflammation, defective insulin signaling, and neuronal dysfunction in Alzheimer’s disease. Alzheimers Dement 2014; 10(1) (Suppl.): S76-83.
[http://dx.doi.org/10.1016/j.jalz.2013.12.010] [PMID: 24529528]
[17]
van Sloten TT, Sedaghat S, Carnethon MR, Launer LJ, Stehouwer CDA. Cerebral microvascular complications of type 2 diabetes: stroke, cognitive dysfunction, and depression. Lancet Diabetes Endocrinol 2020; 8(4): 325-36.
[http://dx.doi.org/10.1016/S2213-8587(19)30405-X] [PMID: 32135131]
[18]
Heringa SM, Bouvy WH, van den Berg E, Moll AC, Kappelle LJ, Biessels GJ. Associations between retinal microvascular changes and dementia, cognitive functioning, and brain imaging abnormalities: A systematic review. J Cereb Blood Flow Metab 2013; 33(7): 983-95.
[http://dx.doi.org/10.1038/jcbfm.2013.58] [PMID: 23591648]
[19]
Crosby-Nwaobi RR, Sivaprasad S, Amiel S, Forbes A. The relationship between diabetic retinopathy and cognitive impairment. Diabetes Care 2013; 36(10): 3177-86.
[http://dx.doi.org/10.2337/dc12-2141] [PMID: 23633523]
[20]
Fickweiler W, Wolfson EA, Paniagua SM, et al. Association of cognitive function and retinal neural and vascular structure in type 1 diabetes. J Clin Endocrinol Metab 2021; 106(4): 1139-49.
[http://dx.doi.org/10.1210/clinem/dgaa921] [PMID: 33378459]
[21]
Exalto LG, Biessels GJ, Karter AJ, Huang ES, Quesenberry CP, Whitmer RA. Severe diabetic retinal disease and dementia risk in type 2 diabetes. J Alzheimers Dis 2014; 42 Suppl 3(03): S109-17.
[http://dx.doi.org/10.3233/JAD-132570] [PMID: 24625797]
[22]
Cheng D, Zhao X, Yang S, Wang G, Ning G. Association between diabetic retinopathy and cognitive impairment: A systematic review and meta-analysis. Front Aging Neurosci 2021; 13: 692911.
[http://dx.doi.org/10.3389/fnagi.2021.692911] [PMID: 34276346]
[23]
Mutlu U, Bonnemaijer PWM, Ikram MA, et al. Retinal neurodegeneration and brain MRI markers: The Rotterdam study. Neurobiol Aging 2017; 60: 183-91.
[http://dx.doi.org/10.1016/j.neurobiolaging.2017.09.003] [PMID: 28974335]
[24]
Gasecka A, Siwik D, Gajewska M, et al. Early biomarkers of neurodegenerative and neurovascular disorders in diabetes. J Clin Med 2020; 9(9): 2807.
[http://dx.doi.org/10.3390/jcm9092807] [PMID: 32872672]
[25]
Diretrizes da Sociedade Brasileira de Diabetes Mellitus 2017– 2018. In. São Paulo, Brasil: Clannad Editora Científica; 2017. Available from: https://diabetes. orgbr/ebook/ diretrizes-dasociedade- brasileira-de-diabetes-2017- 2018/
[26]
World Medical Association. World Medical Association Declaration of Helsinki: Ethical principles for medical research involving human subjects. JAMA 2013; 310(20): 2191-4.
[http://dx.doi.org/10.1001/jama.2013.281053] [PMID: 24141714]
[27]
Seaquist ER, Anderson J, Childs B, et al. Hypoglycemia and diabetes: A report of a workgroup of the American diabetes association and the endocrine society. Diabetes Care 2013; 36(5): 1384-95.
[http://dx.doi.org/10.2337/dc12-2480] [PMID: 23589542]
[28]
Barroso WKS, Rodrigues CIS, Bortolotto LA, et al. Brazilian Guidelines of Hypertension - 2020. Arq Bras Cardiol 2021; 116(3): 516-658.
[http://dx.doi.org/10.36660/abc.20201238] [PMID: 33909761]
[29]
Ting DSW, Cheung GCM, Wong TY. Diabetic retinopathy: global prevalence, major risk factors, screening practices and public health challenges: A review. Clin Exp Ophthalmol 2016; 44(4): 260-77.
[http://dx.doi.org/10.1111/ceo.12696] [PMID: 26716602]
[30]
Wilkinson CP, Ferris FL III, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 2003; 110(9): 1677-82.
[http://dx.doi.org/10.1016/S0161-6420(03)00475-5] [PMID: 13129861]
[31]
Zanocco JA, Nishida SK, Passos MT, et al. Race adjustment for estimating glomerular filtration rate is not always necessary. Nephron Extra 2012; 2(1): 293-302.
[http://dx.doi.org/10.1159/000343899] [PMID: 23243414]
[32]
Levey AS, Stevens LA, Schmid CH, et al. A new equation to estimate glomerular filtration rate. Ann Intern Med 2009; 150(9): 604-12.
[http://dx.doi.org/10.7326/0003-4819-150-9-200905050-00006] [PMID: 19414839]
[33]
KDIGO 2020 Clinical practice guideline for diabetes management in chronic kidney disease. Nephrology and Dialysis 2021; 23(2) (Suppl.): 9-121.
[34]
Mastrocola LE, Amorim BJ, Vitola JV, et al. Update of the Brazilian Guideline on Nuclear Cardiology - 2020. Arq Bras Cardiol 2020; 114(2): 325-429.
[PMID: 32215507]
[35]
Campanholo KR, Romão MA, Machado MAR, et al. Performance of an adult Brazilian sample on the Trail Making Test and Stroop Test. Dement Neuropsychol 2014; 8(1): 26-31.
[http://dx.doi.org/10.1590/S1980-57642014DN81000005] [PMID: 29213876]
[36]
Hamdan AC, Hamdan EMLR. Effects of age and education level on the Trail Making Test in a healthy Brazilian sample. Psychol Neurosci 2009; 2(2): 199-203.
[http://dx.doi.org/10.3922/j.psns.2009.2.012]
[37]
Pavão Martins I, Maruta C, Freitas V, Mares I. Executive performance in older Portuguese adults with low education. Clin Neuropsychol 2013; 27(3): 410-25.
[http://dx.doi.org/10.1080/13854046.2012.748094] [PMID: 23259850]
[38]
Nitrini R, Caramelli P, Bottino CM de C, Damasceno BP, Brucki SM, Anghinah R. Diagnosis of alzheimer’s disease in Brazil: cognitive and functional evaluation. Recommendations of the scientific Department of Cognitive Neurology and Aging of the Brazilian Academy of Neurology. Arq Neuropsiquiatr 2005; 63(3A): 720-7.
[http://dx.doi.org/10.1590/S0004-282X2005000400034] [PMID: 16172733]
[39]
Bertolucci PHF, Okamoto IH, Brucki SMD, Siviero MO, Toniolo Neto J, Ramos LR. Applicability of the CERAD neuropsychological battery to Brazilian elderly. Arq Neuropsiquiatr 2001; 59(3-A): 532-6.
[http://dx.doi.org/10.1590/S0004-282X2001000400009] [PMID: 11588630]
[40]
Fillenbaum GG, van Belle G, Morris JC, et al. Consortium to establish a registry for Alzheimer’s disease (CERAD): The first twenty years. Alzheimers Dement 2008; 4(2): 96-109.
[http://dx.doi.org/10.1016/j.jalz.2007.08.005] [PMID: 18631955]
[41]
Burns A, Brayne C, Folstein M. The mini-mental state examination, will we be using it in 2001? Int J Geriatr Psychiatry 1998; 13(5): 285-94.
[http://dx.doi.org/10.1002/(SICI)1099-1166(199805)13:5<285:AID-GPS753>3.0.CO;2-V] [PMID: 9658260]
[42]
Almeida OP. Mini mental state examination and the diagnosis of dementia in Brazil. Arq Neuropsiquiatr 1998; 56(3B): 605-12.
[http://dx.doi.org/10.1590/S0004-282X1998000400014] [PMID: 9850757]
[43]
Bertolucci PHF, Brucki SMD, Campacci SR, Juliano YO. The Mini-Mental State Examination in a general population: Impact of educational status. Arquivos de Neuro-Psiquiatria 1994; 52(1): 1-7.
[http://dx.doi.org/10.1590/S0004-282X1994000100001]
[44]
Brucki SMD, Nitrini R, Caramelli P, Bertolucci PHF, Okamoto IH. Suggestions for utilization of the mini-mental state examination in Brazil. Arq Neuropsiquiatr 2003; 61(3B): 777-81.
[http://dx.doi.org/10.1590/S0004-282X2003000500014] [PMID: 14595482]
[45]
Kochhann R, Varela JS, Lisboa CSM, Chaves MLF. The mini mental state examination: Review of cutoff points adjusted for schooling in a large Southern Brazilian sample. Dement Neuropsychol 2010; 4(1): 35-41.
[http://dx.doi.org/10.1590/S1980-57642010DN40100006] [PMID: 29213658]
[46]
Passos VMA, Giatti L, Bensenor I, Chor D, Barreto SM. Education plays a greater role than age in cognitive test performance among participants of the Brazilian longitudinal study of adult health (ELSA-Brasil). Int J Epidemiol 2015; 44 (Suppl. 1): i265-5.
[http://dx.doi.org/10.1093/ije/dyv096.503]
[47]
Alencar RC, Cobas RA, Gomes MB. Assessment of cognitive status in patients with type 2 diabetes through the mini-mental status examination: A cross-sectional study. Diabetol Metab Syndr 2010; 2(1): 10.
[http://dx.doi.org/10.1186/1758-5996-2-10] [PMID: 20205826]
[48]
Monteiro S, Torres A, Pereira A, Albuquerque E, Morgadinho R. Preliminary validation study of a Portuguese version of the patient health questionnaire (PHQ-9). Eur Psychiatry 2013; 28(S1): 1.
[http://dx.doi.org/10.1016/S0924-9338(09)71489-0]
[49]
Santos IS, Tavares BF, Munhoz TN, et al. Sensibilidade e especificidade do patient health questionnaire-9 (PHQ-9) entre adultos da população geral. Cad Saude Publica 2013; 29(8): 1533-43.
[http://dx.doi.org/10.1590/S0102-311X2013001200006] [PMID: 24005919]
[50]
Hosmer DW, Lemeshow S. Applied Logistic Regression. New York, Toronto: Wiley 2000; p. 383.
[http://dx.doi.org/10.1002/0471722146]
[51]
Gregg EW, Sattar N, Ali MK. The changing face of diabetes complications. Lancet Diabetes Endocrinol 2016; 4(6): 537-47.
[http://dx.doi.org/10.1016/S2213-8587(16)30010-9] [PMID: 27156051]
[52]
Petersen RC, Lopez O, Armstrong MJ, et al. Practice guideline update summary: Mild cognitive impairment: Report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology. Neurology 2018; 90(3): 126-35.
[http://dx.doi.org/10.1212/WNL.0000000000004826] [PMID: 29282327]
[53]
Langa KM, Levine DA. The diagnosis and management of mild cognitive impairment: A clinical review. JAMA 2014; 312(23): 2551-61.
[http://dx.doi.org/10.1001/jama.2014.13806] [PMID: 25514304]
[54]
Caamaño-Isorna F, Corral M, Montes-Martínez A, Takkouche B. Education and dementia: A meta-analytic study. Neuroepidemiology 2006; 26(4): 226-32.
[http://dx.doi.org/10.1159/000093378] [PMID: 16707907]
[55]
Livingston G, Huntley J, Sommerlad A, et al. Dementia prevention, intervention, and care: 2020 report of the Lancet Commission. Lancet 2020; 396(10248): 413-46.
[http://dx.doi.org/10.1016/S0140-6736(20)30367-6] [PMID: 32738937]
[56]
Díaz-Coránguez M, Ramos C, Antonetti DA. The inner blood-retinal barrier: Cellular basis and development. Vision Res 2017; 139: 123-37.
[http://dx.doi.org/10.1016/j.visres.2017.05.009] [PMID: 28619516]
[57]
Blazes M, Lee CS. Understanding the brain through aging eyes. Advances in Geriatric Medicine and Research 2021; 3(2): e210008.
[PMID: 33748826]
[58]
Zhao W-Q, Chen H, Quon MJ, Alkon DL. Insulin and the insulin receptor in experimental models of learning and memory. Eur J Pharmacol 2004; 490(1-3): 71-81.
[http://dx.doi.org/10.1016/j.ejphar.2004.02.045] [PMID: 15094074]
[59]
Ferrario CR, Reagan LP. Insulin-mediated synaptic plasticity in the CNS: Anatomical, functional and temporal contexts. Neuropharmacology 2018; 136(Pt B): 182-91.
[PMID: 29217283]
[60]
Chiu S-L, Chen C-M, Cline HT. Insulin receptor signaling regulates synapse number, dendritic plasticity, and circuit function in vivo. Neuron 2008; 58(5): 708-19.
[http://dx.doi.org/10.1016/j.neuron.2008.04.014] [PMID: 18549783]
[61]
Ko F, Muthy ZA, Gallacher J, et al. Association of retinal nerve fiber layer thinning with current and future cognitive decline: A study using optical coherence tomography. JAMA Neurol 2018; 75(10): 1198-205.
[http://dx.doi.org/10.1001/jamaneurol.2018.1578] [PMID: 29946685]
[62]
Khawaja AP, Chan MPY, Yip JLY, et al. Retinal nerve fiber layer measures and cognitive function in the EPIC-norfolk cohort study. Invest Ophthalmol Vis Sci 2016; 57(4): 1921-6.
[http://dx.doi.org/10.1167/iovs.16-19067] [PMID: 27092718]
[63]
van Dijk HW, Verbraak FD, Kok PHB, et al. Decreased retinal ganglion cell layer thickness in patients with type 1 diabetes. Invest Ophthalmol Vis Sci 2010; 51(7): 3660-5.
[http://dx.doi.org/10.1167/iovs.09-5041] [PMID: 20130282]
[64]
Ponirakis G, Al Hamad H, Sankaranarayanan A, et al. Association of corneal nerve fiber measures with cognitive function in dementia. Ann Clin Transl Neurol 2019; 6(4): 689-97.
[http://dx.doi.org/10.1002/acn3.746] [PMID: 31019993]
[65]
Al-Janahi E, Ponirakis G, Al Hamad H, et al. Corneal nerve and brain imaging in mild cognitive impairment and dementia. J Alzheimers Dis 2020; 77(4): 1533-43.
[http://dx.doi.org/10.3233/JAD-200678] [PMID: 32925064]
[66]
Ponirakis G, Elsotouhy A, Al Hamad H, et al. Association of cerebral ischemia with corneal nerve loss and brain atrophy in MCI and dementia. Front Neurosci 2021; 15: 690896.
[http://dx.doi.org/10.3389/fnins.2021.690896] [PMID: 34234643]
[67]
Lee CS, Larson EB, Gibbons LE, et al. Associations between recent and established ophthalmic conditions and risk of Alzheimer’s disease. Alzheimers Dement 2019; 15(1): 34-41.
[http://dx.doi.org/10.1016/j.jalz.2018.06.2856] [PMID: 30098888]
[68]
Cheung CY, Ikram MK, Chen C, Wong TY. Imaging retina to study dementia and stroke. Prog Retin Eye Res 2017; 57: 89-107.
[http://dx.doi.org/10.1016/j.preteyeres.2017.01.001] [PMID: 28057562]
[69]
Naël V, Pérès K, Dartigues J-F, et al. Vision loss and 12-year risk of dementia in older adults: The 3C cohort study. Eur J Epidemiol 2019; 34(2): 141-52.
[http://dx.doi.org/10.1007/s10654-018-00478-y] [PMID: 30610413]
[70]
Shang X, Zhu Z, Wang W, Ha J, He M. The association between vision impairment and incidence of dementia and cognitive impairment: A systematic review and meta-analysis. Ophthalmology 2021; 128(8): 1135-49.
[http://dx.doi.org/10.1016/j.ophtha.2020.12.029] [PMID: 33422559]
[71]
Chen SP, Bhattacharya J, Pershing S. Association of vision loss with cognition in older adults. JAMA Ophthalmol 2017; 135(9): 963-70.
[http://dx.doi.org/10.1001/jamaophthalmol.2017.2838] [PMID: 28817745]
[72]
Paik J-S, Ha M, Jung YH, et al. Low vision and the risk of dementia: A nationwide population-based cohort study. Sci Rep 2020; 10(1): 9109.
[http://dx.doi.org/10.1038/s41598-020-66002-z] [PMID: 32499618]
[73]
Michalowsky B, Hoffmann W, Kostev K. Association between hearing and vision impairment and risk of dementia: Results of a case-control study based on secondary data. Front Aging Neurosci 2019; 11: 363.
[http://dx.doi.org/10.3389/fnagi.2019.00363] [PMID: 31920631]
[74]
Hong T, Mitchell P, Burlutsky G, Liew G, Wang JJ. Visual impairment, hearing loss and cognitive function in an older population: Longitudinal findings from the blue mountains eye study. PLoS One 2016; 11(1): e0147646.
[http://dx.doi.org/10.1371/journal.pone.0147646] [PMID: 26808979]
[75]
Wu M, Mei F, Hu K, et al. Diabetic retinopathy and cognitive dysfunction: A systematic review and meta-analysis. Acta Diabetol 2022; 59(4): 443-59.
[http://dx.doi.org/10.1007/s00592-021-01829-0] [PMID: 35112186]
[76]
Chai Y-H, Zhang Y-P, Qiao Y-S, et al. Association between diabetic retinopathy, brain structural abnormalities, and cognitive impairment for accumulated evidence in observational studies. Am J Ophthalmol 2022; 239: 37-53.
[http://dx.doi.org/10.1016/j.ajo.2022.01.011] [PMID: 35063409]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy