Optical and structural properties of biological tissues under diabetes mellitus

Daria K. Tuchina; Valery V. Tuchin

doi:10.18287/JBPE18.04.020201

Authors

Daria K. Tuchina Saratov State University, Russia Tomsk State University, Russia
Valery V. Tuchin Saratov State University, Russia Samara National Research University, Russia Laboratory of Laser Diagnostics of Technical and Living Systems, Institute of Precision Mechanics and Control, Russian Academy of Sciences, Saratov, Russia

DOI:

https://doi.org/10.18287/JBPE18.04.020201

Keywords:

diabetes mellitus, protein glycation, tissues, skin, myocardium, cardiovascular system, optical properties, diffusion of metabolites

Abstract

Diabetes mellitus is a serious social and economic problem of modern society because it is widespread and fraught with numerous complications. Therefore, it is necessary to search for new methods of diabetes mellitus diagnostics and treatment and to improve the existing ones, which, in turn, requires thorough investigation of the disease development mechanisms, as well as elaboration of simple and reliable methods and criteria for detecting the complication precursors. In connection with the solution of these problems, in the paper we present an analytical review of recent publications devoted to the study of the changes of structural and optical properties of biological tissues under the conditions of diabetes mellitus development using in vitro models of glycated tissues, in vivo experimental models of diabetes in laboratory animals, and clinical studies.

References

J. E. Shaw, R. A. Sicree, and P. Z. Zimmet, “Global estimates of the prevalence of diabetes for 2010 and 2030,” Diabetes Research and Clinical Practice 87, 4–14 (2010).

Diabetes Fact Sheet, World Health Organization (2017).

C. D. Mathers, D. Loncar, “Projections of Global Mortality and Burden of Disease from 2002 to 2030,” PLoS Medicine 3(11), e442 (2006).

D. LeRoith, S. I. Taylor, and J. M. Olefsky (Eds.), Diabetes Mellitus: A Fundamental and Clinical Text, 3rd edition, Lippincott Williams & Wilkins (2004).

K. T. Patton, G. A. Thibodeau, The Human Body in Health & Disease, 6th Edition, Elsevier Inc. (2014).

D. G. Gardner, D. M. Shoback, Greenspan's Basic & Clinical Endocrinology, 9th Edition, McGraw-Hill Medical, NY (2011).

B. B. Tripathy, RSSDI Textbook of Diabetes Mellitus, 2nd Edition, Jaypee Brothers Medical Publishers, New Delhi (2012).

Diabetes Care, Volume 40, Supplement 1, American Diabetes Association Inc. (2017).

A. J. King, “The use of animal models in diabetes research,” British Journal of Pharmacology 166, 877–894 (2012).

T. Szkudelski, “The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas,” Physiological Research 50(6), 537–546 (2001).

S. Lenzen, “The mechanisms of alloxan- and streptozotocin-induced diabetes,” Diabetologia 51, 216–226 (2008).

A. Burgeiro, A. Fuhrmann, S. Cherian, D. Espinoza, I. Jarak, R. A. Carvalho, M. Loureiro, M. Patrício, M. Antunes, and E. Carvalho, “Glucose uptake and lipid metabolism are impaired in epicardial adipose tissue from heart failure patients with or without diabetes,” American Journal of Physiology-Endocrinology and Metabolism 310(7), E550–E564 (2016).

V. Vinokur, G. Leibowitz, L. Grinberg, R. Eliashar, E. Berenshtein, and M. Chevion, “Diabetes and the heart: could the diabetic myocardium be protected by preconditioning?” Redox Report 12(6), 246–256 (2007).

T. Nishikawa, D. Edelstein, X. L. Du, S. Yamagishi, T. Matsumura, Y. Kaneda, M. A. Yorek, D. Beebe, P. J. Oates, H. P. Hammes, I. Giardino, and M. Brownlee, “Normalizing mitochondrial superoxide production blocks three pathways of hyperglycemic damage,” Nature 404(6779), 787–790 (2000).

X. Du, T. Matsumura, D. Edelstein, D. Edelstein, L. Rossetti, Z. Zsengellér, C. Szabó, and M. Brownlee, “Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells,” Journal of Clinical Investigation 112(7), 1049–1057 (2003).

M. Chevion, “A site-specific mechanism for free radical induced biological damage: the essential role of redox-active transition metals,” Free Radical Biology and Medicine 5(1), 27–37 (1988).

N. Vigneshwaran, G. Bijukumar, N. Karmakar, S. Anand, and A. Misra, “Autofluorescence characterization of advanced glycation end products of hemoglobin,” Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 61(1–2), 163–170, (2005).

N. I. Dikht, A. B. Bucharskaya, G. S. Terentyuk, G. N. Maslyakova, O. V. Matveeva, N. A. Navolokin, N. G. Khlebtsov, and B. N. Khlebtsov, “Morphological study of the internal organs in rats with alloxan diabetes and transplanted liver tumor after intravenous injectin of gold nanorods,” Russian Open Medical Journal 3(3), 0301 (2014).

D. McGuire, N. Marx, Diabetes in Cardiovascular Disease: A Companion to Braunwald’s Heart Disease, Elsevier Health Sciences (2014).

V. V. Tuchin (Ed.), Handbook of Optical Sensing of Glucose in Biological Fluids and Tissues, Taylor & Francis Group LLC, CRC Press (2009).

H. Ullah, A. Mariampillai, M. Ikram, and I. A. Vitkin, “Can Temporal Analysis of Optical Coherence Tomography Statistics Report on Dextrorotatory-Glucose Levels in Blood?” Laser Physics 21(11), 1962–1971 (2011).

G. Purvinis, B. D. Cameron, and D. M. Altrogge, “Noninvasive polarimetric-based glucose monitoring: an in vivo study,” Journal of Diabetes Science and Technology 5(2), 380–387 (2011).

N. C. Dingari, I. Barman, G. P. Singh, J. W. Kang, R. R. Dasari, and M. S. Feld, “Investigation of the specificity of Raman spectroscopy in non-invasive blood glucose measurements,” Analytical and Bioanalytical Chemistry 400(9), 2871–2880 (2011).

Y. Zhang, G. Wu, H. Wei, Z. Guo, H. Yang, Y. He, S. Xie, and Y. Liu, “Continuous noninvasive monitoring of changes in human skin optical properties during oral intake of different sugars with optical coherence tomography,” Biomedical Optics Express 5(4), 990–999 (2014).

R. Y. He, H. J. Wei, H. M. Gu, Z. G. Zhu, Y. Q. Zhang, X. Guo, and T. Cai, “Effects of optical clearing agents on noninvasive blood glucose monitoring with optical coherence tomography: a pilot study,” Journal of Biomedical Optics 17(10), 101513 (2012).

M. A. Pleitez, T. Lieblein, A. Bauer, O. Hertzberg, H. von Lilienfeld-Toal, and W. Mäntele, “Windowless ultrasound photoacoustic cell for in vivo mid-IR spectroscopy of human epidermis: Low interference by changes of air pressure, temperature, and humidity caused by skin contact opens the possibility for a non-invasive monitoring of glucose in the interstitial fluid,” Review of Scientific Instruments 84(8), 084901 (2013).

N. C. Dingari, I. Barman, J. W. Kang, C. R. Kong, R. R. Dasari, and M. S. Feld, “Wavelength selection-based nonlinear calibration for transcutaneous blood glucose sensing using Raman spectroscopy,” Journal of Biomedical Optics 16(8), 087009 (2011).

J. M. Yuen, N. C. Shah, J. T. Walsh, M. R. Glucksberg, and R. P. Van Duyne, “Transcutaneous glucose sensing by surface-enhanced spatially offset Raman spectroscopy in a rat model,” Analytical Chemistry 82(20), 8382–8385 (2010).

S. Firdous, M. Nawaz, M. Ahmed, S. Anwar, A. Rehman, R. Rashid, and A. Mahmood, “Measurement of diabetic sugar concentration in human blood using Raman spectroscopy,” Laser physics 22(6), 1090–1094 (2012).

X. X. Guo, A. Mandelis, and B. Zinman, “Noninvasive glucose detection in human skin using wavelength modulated differential laser photothermal radiometry,” Biomedical Optics Express 3(11), 3012–3021 (2012).

S. A. A. Shah, A. Laude, I. Faye, and T. B. Tang, “Automated microaneurysm detection in diabetic retinopathy using curvelet transform,” Journal of Biomedical Optics 21(10), 101404 (2016).

Y. J. Heo, S. Takeuchi, “Towards smart tattoos: implantable biosensors for continuous glucose monitoring,” Advanced Healthcare Materials 2(1), 43–56 (2013).

E. Selvin, M. W. Steffes, H. Zhu, K. Matsushita, L. Wagenknecht, J. Pankow, J. Coresh, and F. L. Brancati, “Glycated Hemoglobin, Diabetes, and Cardiovascular Risk in Nondiabetic Adults,” The New England Journal of Medicine 362(9), 800–811 (2010).

J.-Y. Tseng, A. A. Ghazaryan, W. Lo, Y.-F. Chen, V. Hovhannisyan, S.-J. Chen, H.-Y. Tan, and C.-Y. Dong, “Multiphoton spectral microscopy for imaging and quantification of tissue glycation,” Biomedical Optics Express 2(2), 218–230 (2011).

G. Mazarevica, T. Freivalds, and A. Jurka, “Properties of erythrocyte light refraction in diabetic patients,” Journal of Biomedical Optics 7(2), 244–247 (2002).

J. Blackwell, K. M. Katika, L. Pilon, K. M. Dipple, S. R. Levin, and A. Nouvong, “In vivo time-resolved autofluorescence measurements to test for glycation of human skin,” Journal of Biomedical Optics 13(1), 014004 (2008).

U. Kanska, J. Boratynski, “Thermal glycation of proteins by D-glucose and D-fructose,” Archivum Immunologiae et Therapiae Experimentalis 50(1), 61–66 (2002).

O. S. Khalil, “Non-Invasive Glucose Measurement Technologies: An Update from 1999 to the Dawn of the New Millennium,” Diabetes Technology & Therapeutics 6(5), 660–697 (2004).

D. K. Tuchina, R. Shi, A. N. Bashkatov, E. A. Genina, D. Zhu, Q. Luo, and V. V. Tuchin, “Ex vivo optical measurements of glucose diffusion kinetics in native and diabetic mouse skin,” Journal of Biophotonics 8(4), 332-346 (2015).

D. K. Tuchina, A. N. Bashkatov, A. B. Bucharskaya, E. A. Genina, and V. V. Tuchin, “Study of glycerol diffusion in skin and myocardium ex vivo under the conditions of developing alloxan-induced diabetes,” Journal of Biomedical Photonics & Engineering 3(2), 020302 (2017).

T. Pan, M. Li, J. Chen, and H. Xue, “Quantification of glycated hemoglobin indicator HbA1c through near-infrared spectroscopy,” Journal of Innovative Optical Health Sciences 7(4), 1350060 (2014).

E. Shirshin, O. Cherkasova, T. Tikhonova, E. Berlovskaya, A. Priezzhev, and V. Fadeev, “Native fluorescence spectroscopy of blood plasma of rats with experimental diabetes: identifying fingerprints of glucose-related metabolic pathways,” Journal of Biomedical Optics 20(5), 051033 (2015).

G. V. Maksimov, O. G. Luneva, N. V. Maksimova, E. Matettuchi, E. A. Medvedev, V. Z. Pashchenko, and A. B. Rubin. “Role of viscosity and permeability of the erythrocyte plasma membrane in changes in oxygen-binding properties of hemoglobin during diabetes mellitus,” Bulletin of Experimental Biology and Medicine, 140(5), 510–513 (2005).

J. F. Villa-Manríquez, J. Castro-Ramos, F. Gutiérrez-Delgado, M. A. Lopéz-Pacheco, and A. E. Villanueva-Luna, “Raman spectroscopy and PCA-SVM as a non-invasive diagnostic tool to identify and classify qualitatively glycated hemoglobin levels in vivo,” Journal of Biophotonics 10(8), 1074–1079 (2016).

P. A. Timoshina, A. B. Bucharskaya, D. A. Alexandrov, and V. V. Tuchin, “Study of blood microcirculation of pancreas in rats with alloxan diabetes by Laser Speckle Contrast Imaging,” Journal of Biomedical Photonics & Engineering 3(2), 020301 (2017).

F. Wei, S. Rui, and D. Zhu, “Monitoring skin microvascular dysfunction of type 1 diabetic mice using in vivo skin optical clearing,” Proceedings of SPIE 10493, 104931O (2018).

O. A. Smolyanskaya, I. J. Schelkanova, M. S. Kulya, E. L. Odlyanitskiy, I. S. Goryachev, A. N. Tcypkin, Y. V. Grachev, Ya. G. Toropova, and V. V. Tuchin, “Glycerol dehydration of native and diabetic animal tissues studied by THz-TDS and NMR methods,” Biomedical optics express 9(3), 1198 (2018).

V. V. Tuchin, Optical Clearing of Tissues and Blood, PM 154, SPIE Press, Bellingham, WA (2006).

D. Zhu, K. V. Larin, Q. Luo, and V. V. Tuchin, “Recent progress in tissue optical clearing,” Laser & Photonics Reviews 7(5), 732–757 (2013).

L. M. Oliveira, M. I. Carvalho, E. Nogueira, and V. V. Tuchin, “The characteristic time of glucose diffusion measured for muscle tissue at optical clearing,” Laser Physics 23(7), 075606 (2013).

L. Oliveira, M. I. Carvalho, E. Nogueira, and V. V. Tuchin, “Optical measurement of rat muscle samples under treatment with ethylene glycol and glucose,” Journal of Innovative Optical Health Sciences 6(2), 1350012 (2013).

M. G. Ghosn, N. Sudheendran, M. Wendt, A. Glasser, V. V. Tuchin, and K. V. Larin, “Monitoring of glucose permeability in monkey skin in vivo using Optical Coherence Tomography,” Journal of Biophotonics 3(1–2), 25–33 (2010).

A. N. Bashkatov, E. A. Genina, Yu. P. Sinichkin, V. I. Kochubey, N. A. Lakodina, and V. V. Tuchin, “Glucose and mannitol diffusion in human dura mater,” Biophysical Journal 85(5), 3310–3318 (2003).

M. Kreft, M. Luksic, T. M. Zorec, M. Prebil, and R. Zorec, “Diffusion of D–glucose measured in the cytosol of a single astrocyte,” Cellular and Molecular Life Sciences 70(8), 1483–1492 (2012).

M. G. Ghosn, E. F. Carbajal, N. A. Befrui, and K. V. Larin, “Permeability of Hyperosmotic Agent in Normal and Atherosclerotic Vascular Tissues,” Journal Of Biomedical Optics 13(1), 010505 (2008).

X. Guo, G. Wu, H. Wei, X. Deng, H. Yang, Y. Ji, Y. He, Z. Guo, S. Xie, H. Zhong, Q. Zhao, and Z. Zhu, “Quantification of Glucose Diffusion in Human Lung Tissues by Using Fourier Domain Optical Coherence Tomography,” Photochemistry and Photobiology 88(2), 311–316 (2012).

F. Quondamatteo, “Skin and diabetes mellitus: what do we know?” Cell and Tissue Research 355(1), 1–21 (2014).

G. M. Campos de Macedo, S. Nunes, and T. Barreto, “Skin disorders in diabetes mellitus: an epidemiology and physiopathology,” Diabetology & Metabolic Syndrome 8(1), 63 (2016)

J. A. Suaya, D. F. Eisenberg, C. Fang, and L. G. Miller, “Skin and Soft Tissue Infections and Associated Complications among Commercially Insured Patients Aged 0–64 Years with and without Diabetes in the U.S.,” PLOS One 8(4), e60057 (2013).

M. Marre, “Genetics and the prediction of complications in type 1 diabetes,” Diabetes Care 22(2), B53–B58 (1999).

I. J. Goldberg, “Why does diabetes increase atherosclerosis? I don’t know!” Journal of Clinical Investigation 114(5), 613–615 (2004).

W. W. Song, A. Ergul, “Type-2 diabetes-induced changes in vascular extracellular matrix gene expression: Relation to vessel size,” Cardiovascular Diabetology 5, 3 (2006).

G. Spinetti, N. Kraenkel, C. Emanueli, and P. Madeddu, “Diabetes and vessel wall remodelling: from mechanistic insights to regenerative therapies,” Cardiovascular Research 78(2), 265–273 (2008).

D. Pedicino, A. F. Giglio, V. A. Galiffa, F. Trotta and G. Liuzzo, “Type 2 Diabetes, Immunity and Cardiovascular Risk: A Complex Relationship,” Chap. 3 in Pathophysiology and Complications of Diabetes Mellitus, O. O. Oguntibeju (Ed.), InTech (2012).

M. S. Anderson, J. A. Bluestone, “The NOD mouse: a model of immune dysregulation,” Annual Review of Immunology 23(1), 447–485 (2005).

J. A. Bluestone, K. Herold, and G. Eisenbarth, “Genetics, pathogenesis and clinical interventions in type 1 diabetes,” Nature 464(7293), 1293–1300 (2010).

S. Makino, K. Kunimoto, Y. Muraoka, Y. Mizushima, K. Katagiri, and Y. Tochino, “Breeding of a non-obese, diabetic strain of mice,” Experimental Animals 29(1), 1–13 (1980).

T. T. Berezov, B. F. Korovkin, Biological Chemistry, Meditsina, Moscow (1998) [in Russian].

B. Coudrillier, J. Pijanka, J. Jefferys, T. Sorensen, H. A. Quigley, C. Boote, and T. D. Nguyen, “Collagen Structure and Mechanical Properties of the Human Sclera: Analysis for the Effects of Age,” Journal of Biomechanical Engineering 137(4), 041006 (2015).

M. Maciążek-Jurczyk, A. Szkudlarek, M. Chudzik, J. Pożycka, and A. Sułkowska, “Alteration of human serum albumin binding properties induced by modifications: A review,” Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy 188, 675–683 (2018).

S. F. Diniz, F. P. L. G. Amorim, F. F. Cavalcante-Neto, A. L. Bocca, A. C. Batista, G. E. P. M. Simm, and T. A. Silva, “Alloxan-induced diabetes delays repair in a rat model of closed tibial fracture,” Brazilian Journal Of Medical and Biological Research 41(5), 373–379 (2008).

D. Dufrane, M. van Steenberghe, Y. Guiot, R. M. Goebbels, A. Saliez, and P. Gianello, “Streptozotocin-induced diabetes in large animals (pigs/primates): role of GLUT2 transporter and beta-cell plasticity,” Transplantation 81(1), 36–45 (2006).

L. M. Hansen, D. Gupta, G. Joseph, D. Weiss, and W. R. Taylor, “The receptor for advanced glycation end products impairs collateral formation in both diabetic and non-diabetic mice,” Laboratory Investigation 97(1), 34–42 (2017).

H. Yu, J. Zhen, B. Pang, J. Gu, and S. Wu, “Ginsenoside Rg1 ameliorates oxidative stress and myocardial apoptosis in streptozotocin-induced diabetic rats,” Journal of Zhejiang University-SCIENCE B, 16(5), 344–354 (2015).

J. Wu, L. Yan, “Streptozotocin-induced type 1 diabetes in rodents as a model for studying mitochondrial mechanisms of diabetic β cell glucotoxicity,” Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy 8, 181–188 (2015).

M. I. Asrarov, M. K. Pozilov, N. A. Ergashev, and M. M. Rakhmatullaeva, “The influence of the hypoglycemic agent glycorazmulin on the functional state of mitochondria in the rats with streptozotocin-induced diabetes,” Problems of Endocrinology 60(3), 38–42 (2014) [in Russian].

L. Dancakova, T. Vasilenko, I. Kova, K. Jakubcova, M. Holly, V. Revajova, F. Sabol, Z. Tomori, M. Iversen, P. Gal, and J. M. Bjordal, “Low-Level Laser Therapy with 810 nm Wavelength Improves Skin Wound Healing in Rats with Streptozotocin-Induced Diabetes,” Photomedicine and Laser Surgery 32(4), 198–204 (2014).

D. E. Kelley, J. He, E. V. Menshikova, and V. B. Ritov, “Dysfunction of Mitochondria in Human Skeletal Muscle in Type 2 Diabetes,” Diabetes 51(10), 2944–2950 (2002).

C. Moran, G. Münch, J. M. Forbes, R. Beare, L. Blizzard, A. J. Venn, T. G. Phan, J. Chen, and V. Srikanth, “Type 2 Diabetes, Skin Autofluorescence, and Brain Atrophy,” Diabetes 64(1), 279–283 (2015).

D. Ziegler, N. Papanas, A. Zhivov, S. Allgeier, K. Winter, I. Ziegler, J. Brüggemann, A. Strom, S. Peschel, B. Köhler, O. Stachs, R. F. Guthoff, and M. Roden, “Early Detection of Nerve Fiber Loss by Corneal Confocal Microscopy and Skin Biopsy in Recently Diagnosed Type 2 Diabetes,” Diabetes 63(7), 2454–2463 (2014).

M. F. Chowdhry, H. A. Vohra, and M. Galiñanes, “Diabetes increases apoptosis and necrosis in both ischemic and nonischemic human myocardium: Role of caspases and poly–adenosine diphosphate–ribose polymerase,” The Journal of Thoracic and Cardiovascular Surgery 134(1), 124–131 (2007).

V. M. Monnier, D. R. Sell, C. Strauch, W. Sun, J. M. Lachin, P. A. Cleary, S. Genuth, and the DCCT Research Group, “The association between skin collagen glucosepane and past progression of microvascular and neuropathic complications in type 1 diabetes,” Diabetes Complications 27(2), 141–149 (2013).

J. R. Acosta, I. Douag, D. P. Andersson, J. Bäckdahl, M. Rydén, P. Arner, and J. Laurencikiene, “Increased fat cell size: a major phenotype of subcutaneous white adipose tissue in non-obese individuals with type 2 diabetes,” Diabetologia 59(3), 560–570 (2016).

E. V. Zharkikh, V. V. Dremin, M. A. Filina, I. N. Makovik, E. V. Potapova, E. A. Zherebtsov, A. I. Zherebtsova, and A. V. Dunaev, “Application of optical non-invasive methods to diagnose the state of the lower limb tissues in patients with diabetes mellitus,” Journal of Physics: Conference Series 929, 012069 (2017).

V. Dremin, E. Zherebtsov, V. Sidorov, A. Krupatkin, I. Makovik, A. Zherebtsova, E. Zharkikh, E. Potapova, A. Dunaev, A. Doronin, A. Bykov, I. Rafailov, K. Litvinova, S. Sokolovski, and E. Rafailov, “Multimodal optical measurement for study of lower limb tissue viability in patients with diabetes mellitus,” Journal of Biomedical Optics 22(8), 085003 (2017).

E. V. Potapova, V. V. Dremin, E. A. Zherebtsov, I. N. Makovik, E. V. Zharkikh, A. V. Dunaev, O. V. Pilipenko, V. V. Sidorov, and A. I. Krupatkin, “A complex approach to noninvasive estimation of microcirculatory tissue impairments in feet of patients with diabetes mellitus using spectroscopy,” Optics and spectroscopy 123(6), 955–964 (2017).

L. A. Muir, C. K. Neeley, K. A. Meyer, N. A. Baker, A. M. Brosius, A. R. Washabaugh, O. A. Varban, J. F. Finks, B. F. Zamarron, C. G. Flesher, J. S. Chang, J. B. DelProposto, L. Geletka, G. Martinez-Santibanez, N. Kaciroti, C. N. Lumeng, and R. W. O’Rourke, “Adipose Tissue Fibrosis, Hypertrophy, and Hyperplasia: Correlations with Diabetes in Human Obesity,” Obesity 24(3), 597–605 (2016).

P. Martín-Mateos, F. Dornuf, B. Duarte, B. Hils, A. Moreno-Oyervides, O. Elias Bonilla-Manrique, F. Larcher, V. Krozer, and P. Acedo, “In-vivo, non-invasive detection of hyperglycemic states in animal models using mm-wave spectroscopy,” Scientific Reports 6(1), 34035 (2016).

A. Rohilla, S. Ali, “Alloxan Induced Diabetes: Mechanisms and Effects,” International journal of research in pharmaceutical and biomedical sciences 3(2), 819–823 (2012).

R. Bansal, N. Ahmad, and J. R. Kidwai, “Alloxan-glucose interaction: effect on incorporation of 14C-leucine into pancreatic islets of rat,” Acta Diabetologica Latina 17(2), 135–143 (1980).

J. H. Lee, S. H. Yang, J. M. Oh, and M. G. Lee, “Pharmacokinetics of drugs in rats with diabetes mellitus induced by alloxan or streptozocin: comparison with those in patients with type I diabetes mellitus,” Journal of Pharmacy and Pharmacology 62(1), 1–23 (2010).

J. R. Garrett, J. Ekström, and L. C. Anderson (Eds.), Frontiers of Oral Biology: Glandular Mechanisms of Salivary Secretion, 10 (1998).

N. Rakieten, M. L. Rakieten, and M. V. Nadkarni, “Studies on the diabetogenic action of streptozotocin,” Cancer Chemotherapy Reports 29, 91–98 (1963).

K. Srinivasan, P. Ramarao, “Animal models in type 2 diabetes research: an overview,” Indian Journal of Medical Research 125, 451–472 (2007).

Y. Dekel, Y. Glucksam, I. Elron-Gross, and R. Margalit, “Insights into modeling streptozotocin-induced diabetes in ICR mice,” Lab Animal 38(2), 55–60 (2009).

K. Hayashi, R. Kojima, and M. Ito, “Strain differences in the diabetogenic activity of streptozotocin in mice,” Biological & Pharmaceutical Bulletin 29(6), 1110–1119 (2006).

M. Elsner, M. Tiedge, and S. Lenzen, “Mechanism underlying resistance of human pancreatic beta cells against toxicity of streptozotocin and alloxan,” Diabetologia 46(12), 1713–1714 (2003).

Y. Yang, P. Santamaria, “Lessons on autoimmune diabetes from animal models,” Clinical Science 110(6), 627–639 (2006).

T. Hanafusa, J. Miyagawa, H. Nakajima, K. Tomita, M. Kuwajima, Y. Matsuzawa, and S. Tarui, “The NOD mouse,” Diabetes Research and Clinical Practice 24, S307–S311 (1994).

J. P. Mordes, R. Bortell, E. P. Blankenhorn, A. A. Rossini, and D. L. Greiner, “Rat models of type 1 diabetes: genetics, environment, and autoimmunity,” ILAR Journal 45(3), 278–291 (2004).

X. Wang, D. C. DuBois, S. Sukumaran, V. Ayyar, W. J. Jusko, and R. R Almon, “Variability in Zucker diabetic fatty rats: differences in disease progression in hyperglycemic and normoglycemic animals,” Diabetes, Metabolic Syndrome and Obesity: Targets and Therapy 7, 531–541 (2014).

S. Yoshida, H. Tanaka, H. Oshima, T. Yamazaki, Y. Yonetoku, T. Ohishi, T. Matsui, and M. Shibasaki, “AS1907417, a novel GPR119 agonist, as an insulinotropic and beta-cell preservative agent for the treatment of type 2 diabetes,” Biochemical and Biophysical Research Communications 400(4), 745–751 (2010).

V. A. Gault, B. D. Kerr, P. Harriott, and P. R. Flatt, “Administration of an acylated GLP-1 and GIP preparation provides added beneficial glucose-lowering and insulinotropic actions over single incretins in mice with Type 2 diabetes and obesity,” Clinical Science 121(3), 107–117 (2011).

J. S. Park, S. D. Rhee, N. S. Kang, W. H. Jung, H. Y. Kim, J. H. Kim, S. K. Kang, H. G. Cheon, J. H. Ahn, and K. Y. Kim, “Anti-diabetic and anti-adipogenic effects of a novel selective 11beta-hydroxysteroid dehydrogenase type 1 inhibitor, 2-(3-benzoyl)-4-hydroxy-1,1-dioxo-2H-1,2-benzothiazine-2-yl-1-phenylethanone (KR-66344),” Biochemical Pharmacology 81(8), 1028–1035 (2011).

P. Lindstrom, “The physiology of obese-hyperglycemic mice [ob/ob mice],” Scientific world journal 7, 666–685 (2007).

T. Bock, B. Pakkenberg, and K. Buschard, “Increased islet volume but unchanged islet number in ob/ob mice,” Diabetes 52(7), 1716–1722 (2003).

F. F. Chehab, M. E. Lim, and R. Lu, “Correction of the sterility defect in homozygous obese female mice by treatment with the human recombinant leptin,” Nature Genetics 12(3), 318–320 (1996).

H. Chen, O. Charlat, L. A. Tartaglia, E. A. Woolf, X. Weng, S. J. Ellis, N. D. Lakey, J. Culpepper, K. J. More, R. E. Breitbart, G. M. Duyk, R. I. Tepper, and J. P. Morgenstern, “Evidence that the diabetes gene encodes the leptin receptor: identification of a mutation in the leptin receptor gene in db/db mice,” Cell 84(3), 491–495 (1996).

A. Pick, J. Clark, C. Kubstrup, M. Levisetti, W. Pugh, S. Bonner-Weir, and K. S. Polonsky, “Role of apoptosis in failure of beta-cell mass compensation for insulin resistance and beta-cell defects in the male Zucker diabetic fatty rat,” Diabetes 47(3), 358–364 (1998).

T. Shibata, S. Takeuchi, S. Yokota, K. Kakimoto, F. Yonemori, and K. Wakitani, “Effects of peroxisome proliferator-activated receptor-alpha and -gamma agonist, JTT-501, on diabetic complications in Zucker diabetic fatty rats,” British Journal of Pharmacology 130(3), 495–504 (2000).

V. M. Monnier, D. R. Sell, “Prevention and repair of protein damage by the Maillard reaction in vivo,” Rejuvenation Research 9(2), 264-273 (2006).

Q. A. Kleter, J. J. M. Damen, M. J. Buijs, and J. M. Ten Cate, “The Maillard reaction in demineralized dentin in vitro,” European Journal of Oral Sciences 105(3), 278-284 (1997).

A. Ioannou, C. Varotsis, “Modifications of hemoglobin and myoglobin by Maillard reaction products (MRPs),” PLoS ONE 12(11), e0188095 (2017).

R. D. G. Leslie, D. C. Robbins (Eds.), Diabetes: Clinical Science in Practice, Cambridge University Press (1995).

A. M. Schmidt, O. Hori, J. X. Chen, J. F. Li, J. Crandall, J. Zhang, R. Cao, S. D. Yan, J. Brett, and D. Stem, “Advanced Glycation Endproducts Interacting with Their Endothelial Receptor Induce Expression of Vascular Cell Adhesion Molecule-1 (VCAM-1) in Cultured Human Endothelial Cells and in Mice. A Potential Mechanism for the Accelerated Vasculopathy of Diabetes,” Journal of Clinical Investigation 96, 1395–1403 (1995).

J. Kinnunen, H. T. Kokkonen, V. Kovanen, M. Hauta-Kasari, P. Vahimaa, M. J. Lammi, J. Töyräs, and J. S. Jurvelinb, “Nondestructive fluorescence-based quantification of threose-induced collagen cross-linking in bovine articular cartilage,” Journal of Biomedical Optics 17(9), 0970031 (2012).

G. T. Wondrak, M. J. Roberts, D. Cervantes-Laurean, M. K. Jacobson, and E. L. Jacobson, “Proteins of the extracellular matrix are sensitizers of photo-oxidative stress in human skin cells,” Journal of Investigative Dermatology 121(3), 578–586 (2003).

M. Yokota, Y. Tokudome, “The Effect of Glycation on Epidermal Lipid Content, Its Metabolism and Change in Barrier Function,” Skin Pharmacology and Physiology 29(5), 231–242 (2016).

E. L. Hull, M. N. Ediger, A. N. T. Unione, E. K. Deemer, M. L. Stroman, and J. W. Baynes, “Noninvasive, optical detection of diabetes: model studies with porcine skin,” Optics Express 12(19), 4496–4510 (2004).

V. M. Monnier, W. Sun, X. Gao, D. R Sell, P. A. Cleary, J. M. Lachin, S. Genuth, and The DCCT/EDIC Research Group, “Skin collagen advanced glycation endproducts (AGEs) and the long‑term progression of sub‑clinical cardiovascular disease in type 1 diabetes,” Cardiovascular Diabetology 14, 118 (2015).

S. Genuth, W. Sun, P. Cleary, X. Gao, D. R. Sell, J. Lachin, and V. M. Monnier, “Skin Advanced Glycation End Products Glucosepane and Methylglyoxal Hydroimidazolone Are Independently Associated With Long-term Microvascular Complication Progression of Type 1 Diabetes,” Diabetes 64(1), 266–278 (2015).

O. S. Zhernovaya, V. V. Tuchin, and I. V. Meglinski, “Monitoring of blood proteins glycation,” Laser Physics Letters 5(6), 460–464 (2008).

B.-M. Kim, J. Eichler, K. M. Reiser, A. M. Rubenchik, and L. B. Da Silvam, “Collagen structure and nonlinear susceptibility: effects of heat, glycation, and enzymatic cleavage on second harmonic signal intensity,” Lasers in Surgery and Medicine 27(4), 329–335 (2000).

B. Gopalkrishnapillai, V. Nadanathangam, N. Karmakar, S. Anand, and A. Misra, “Evaluation of autofluorescent property of hemoglobin-advanced glycation end product as a long-term glycemic index of diabetes,” Diabetes 52(4), 1041–1046 (2003).

Y.-J. Hwang, J. Granelli, and J. Lyubovitsky, “Multiphoton optical image guided spectroscopy method for characterization of collagen-based materials modified by glycation,” Analytical Chemistry 83(1), 200–206 (2011).

P. A. Cleary, B. H. Braffett, T. Orchard, T. J. Lyons, J. Maynard, C. Cowie, R. A. Gubitosi-Klug, J. Way, K. Anderson, A. Barnie, and S. Villavicencio, “Clinical and Technical Factors Associated with Skin Intrinsic Fluorescence in Subjects with Type 1 Diabetes from the Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Study,” Diabetes Technology & Therapeutics 15(6), 466–474 (2013).

E. Sugisawa, J. Miura, Y. Iwamoto, and Y. Uchigata, “Skin Autofluorescence Reflects Integration of Past Long-Term Glycemic Control in Patients With Type 1 Diabetes,” Diabetes Care 36(8), 2339–2345 (2013).

J. D. Maynard, M. N. Ediger, R. D Johnson, and M. R. Robinson, Determination of a measure of a glycation end-product or disease state using a flexible probe to determine tissue fluorescence of various sites, Patent US11677498 USA, MPK А61В 6/00, Assignee: VeraLight, Inc., Albuquerque, NM (US), Appl. No.: 11/677,498 (2012).

J. Lin, J. Lin, Z. Huang, P. Lu, J. Wang, X. Wang, and R. Chen, “Raman spectroscopy of human hemoglobin for diabetes detection,” Journal of Innovative Optical Health Sciences 7(1), 1350051 (2014).

K. Sangkyu, L. Joonhyung, Noninvasive apparatus and method for testing glycated hemoglobin, Patent 9841415, Assignee: Samsung Electronics Co., Ltd. (Suwon-si, KR), United States (2017).

M. Mallya, R. Shenoy, G. Kodyalamoole, M. Biswas, J. Karumathil, and S. Kamath, “Absorption Spectroscopy for the Estimation of Glycated Hemoglobin (HbA1c) for the Diagnosis and Management of Diabetes Mellitus: A Pilot Study,” Photomedicine and Laser Surgery 31(5), 219–224 (2013).

T. Pan, M. Li, J. Chen, and H. Xue, “Quantification of glycated hemoglobin indicator HbA1c through near-infrared spectroscopy,” Journal of Innovative Optical Health Sciences 7(4), 1350060 (2014).

M. Rendell, T. Bergman, G. O’Donnell, E. Drobny, J. Borgos, and R. Bonnor, “Microvascular blood flow, volume, and velocity, measured by laser Doppler techniques in IDDM,” Diabetes 38(7), 819–824 (1989).

H. M. Raabe, H. Molsen, S.-M. Mlinaric, Y. Acil, G. H. G. Sinnecker, H. Notbohm, K. Kruse, and P. K. Muller, “Biochemical alterations in collagen IV induced by in vitro glycation,” Biochemical Journal 319(3), 699–704 (1996).

O. S. Zhernovaya, A. N. Bashkatov, E. A. Genina, V. V. Tuchin, I. V. Meglinski, D. Yu. Churmakov, and L. J. Ritchie, “Investigation of glucose-hemoglobin interaction by optical coherence tomography,” Proceedings of SPIE 6535, 65351C (2007).

E. I. Galanzha, A. V. Solovieva, V. V. Tuchin, R. K. Wang, and S. G. Proskurin, “Application of optical coherence tomography for diagnosis and measurements of glycated hemoglobin,” Proceedings of SPIE 5140, 125–132 (2003).

V. V. Tuchin, R. K. Wang, E. I. Galanzha, J. B. Elder, and D. M. Zhestkov, “Monitoring of glycated hemoglobin by OCT measurement of refractive index,” Proceedings of SPIE 5316, 66–77 (2004).

P. J. Higgins, H. F. Bunn, “Kinetic analysis of the nonenzymatic glycosylation of hemoglobin,” The Journal of Biological Chemistry 256(10), 05204–5208 (1981).

G. K. Reddy, “Cross-Linking in Collagen by Nonenzymatic Glycation Increases the Matrix Stiffness in Rabbit Achilles Tendon,” Experimental Diabesity Research 5(2), 143–153 (2004).

B. E. Sherlock, J. N. Harvestine, D. Mitra, A. Haudenschild, J. Hu, K. A. Athanasiou, J. K. Leach, and L. Marcua, “Nondestructive assessment of collagen hydrogel cross-linking using time-resolved autofluorescence imaging,” Journal of Biomedical Optics 23(3), 036004 (2018)

M. Mernea, A. Ionescu, I. Vasile, C. Nica, G. Stoian, T. Dascalu, and D. F. Mihailescu, “In vitro human serum albumin glycation monitored by Terahertz spectroscopy,” Optical and Quantum Electronics 47(4), 961–973 (2015).

A. Goldin, J. A. Beckman, A. M. Schmidt, and M. A. Creager, “Advanced Glycation End Products Sparking the Development of Diabetic Vascular Injury,” Circulation 114(6), 597–605 (2006).

V. L. Emanuel, I. Yu. Karyagina, and Yu. V. Emanuel, “Comparison of method for determining glycosylated hemoglobin,” Laboratornaya meditsina 5, 98–104 (2002) [in Russian].

V. V. Tuchin, Lasers and Fibre Optics in Biomedical Science, Fizmatlit, Moscow (2010) [in Russian].

V. V. Tuchin, Optics of Biological Tissues. Methods of Light Scattering in Medical Diagnostics, Fizmatlit, Moscow (2012) [in Russian].

J. Wang, N. Ma, R. Shi, Y. Zhang, T. Yu, and D. Zhu, “Sugar-induced skin optical clearing: from molecular dynamics simulation to experimental demonstration,” IEEE Journal of Selected Topics in Quantum Electronics 20(2), 256–262 (2014).

E. A. Genina, A. N. Bashkatov, and V. V. Tuchin, “Tissue optical immersion clearing,” Expert Review of Medical Devices 7(6), 825–842 (2010).

F. S. Pavone, P. J. Campagnola (Eds.), “SHG and Optical Clearing,” Chap. 8 in Second Harmonic Generation Imaging, CRC Press, Taylor & Francis Group, Boca Raton, London, NY, 169−189 (2014).

E. A. Genina, A. N. Bashkatov, K. V. Larin, and V. V. Tuchin, “Light–Tissue Interaction at Optical Clearing,” Chap. 7 in Laser Imaging and Manipulation in Cell Biology, F.S. Pavone (Ed.), Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, 113–164 (2010).

L. Shi, L.A. Sordillo, A. Rodriguez-Contreras, and R. Alfano, “Transmission in near-infrared optical windows for deep brain imaging,” Journal of Biophotonics 9(1–2), 38–43 (2015).

D. C. Sordillo, L. A. Sordillo, P. P. Sordillo, and R. R. Alfano, “Fourth Near-Infrared Optical Window for Assessment of Bone and other Tissues,” Proceedings of SPIE 9689, 96894J (2016).

L. A. Sordillo, Y. Pu, S. Pratavieira, Y. Budansky, and R. R. Alfano, “Deep optical imaging of tissue using the second and third near-infrared spectral windows,” Journal of Biomedical Optics, 19(5), 056004 (2014).

S. Y. Lee, H. J. Park, K. Kim, Y. H. Sohn, S. Jang, and Y. K. Park, “Refractive index tomograms and dynamic membrane fluctuations of red blood cells from patients with diabetes mellitus,” Scientific Reports 7(1), 1039 (2017).

R. M. A. Henry, P. J. Kostense, A. M. W. Spijkerman, J. M. Dekker, G. Nijpels, R. J. Heine, O. Kamp, N. Westerhof, L. M. Bouter, and C. D. A. Stehouwer, “Arterial Stiffness Increases With Deteriorating Glucose Tolerance Status,” Circulation 107(16), 2089–2095 (2003).

E. Danese, M. Montagnana, A. Nouvenne, and G. Lippi, “Advantages and Pitfalls of Fructosamine and Glycated Albumin in the Diagnosis and Treatment of Diabetes,” Journal of Diabetes Science and Technology 9(2), 169–176 (2015).

A. Yuen, C. Laschinger, I. Talior, W. Lee, M. Chan, J. Birek, E. W. K. Young, K. Sivagurunathan, E. Won, C. A. Simmons, and C. A. McCulloch, “Methylglyoxal-modified collagen promotes myofibroblast differentiation,” Matrix Biology 29(6), 537–548 (2010).

A. Ghazaryan, M. Omar, G. J. Tserevelakis, and V. Ntziachristos, “Optoacoustic detection of tissue glycation,” Biomedical Optics Express 6(9), 3149 (2015).

M. Gniadecka, O. F. Nielsen, S. Wessel, M. Heidenheim, D. H. Christensen, and H. C. Wulf, “Water and protein structure in photoaged and chronically aged skin,” Journal of Investigative Dermatology 111(6), 1129–1133 (1998).

D. K. Tuchina, A. N. Bashkatov, E. A. Genina, and V. V. Tuchin, Biosensor for noninvasive optical monitoring of the pathology of biological tissues, Patent RF No. 2633494, MPK A61B 5/05, G01N 21/01, Patent holder: N.G. Chernyshevsky Saratov State University, Application No. 2016102046, 22.01.2016, Bul. No. 29 (2017).

L. M. Oliveira, M. I. Carvalho, E. M. Nogueira, and V. V. Tuchin, “Diffusion characteristics of ethylene glycol in skeletal muscle,” Journal of Biomedical Optics 20(5), 051019 (2015).

J.-M. Andanson, K. L. A. Chan, and S. G. Kazarian, “High-throughput spectroscopic imaging applied to permeation through the skin,” Applied Spectroscopy 63(5), 512–517 (2009).

M. J. Choi, H. I. Maibach, “Elastic vesicles as topical/transdermal drug delivery systems,” International Journal of Cosmetic Science 27(4), 211–221 (2005).

N. Akhtar, “Vesicles: a recently developed novel carrier for enhanced topical drug delivery,” Current Drug Delivery 11(1), 87–97 (2014).

L. C. Freitas Lima, V. Andrade Braga, M. S. França Silva, J. Campos Cruz, S. H. Sousa Santos, M. M. Oliveira Monteiro, and C. Moura Balarini, “Adipokines, diabetes and atherosclerosis: an inflammatory association,” Frontiers in Physiology 6, 304 (2015).

D. Schweitzer, L. Deutsch, M. Klemm, S. Jentsch, M. Hammer, S. Peters, J. Haueisen, U. A. Müller, and J. Dawczynskid, “Fluorescence lifetime imaging ophthalmoscopy in type 2 diabetic patients who have no signs of diabetic retinopathy,” Journal of Biomedical Optics 20(6), 061106 (2015).

C. Ghosh, P. Mukhopadhyay, S. Ghosh, and M. Pradhan, “Insulin sensitivity index (ISI0,120) potentially linked to carbon isotopes of breath CO2 for prediabetes and type 2 diabetes,” Scientific Reports 5(1), 11959 (2015).

C.-M. Cheng, Y.-F. Chang, H.-C. Chiang, and C.-W. Chang, “Optical coherence tomography for the structural changes detection in aging skin,” Proceedings of SPIE 10456, 104565B (2018).

D. G. Dyer, J. A. Dunn, S. R. Thorpe, K. E. Bailie, T. J. Lyons, D. R. McCance, and J. W. Baynes, “Accumulation of Maillard Reaction Products in Skin Collagen in Diabetes and Aging,” Journal of Clinical Investigation 91(6), 2463 (1993).

S. Sakai, K. Kikuchi, J. Satoh, H. Tagami, and S. Inoue, “Functional properties of stratum corneum in patients with diabetes mellitus: similarities to senile xerosis,” British Journal of Dermatology 153(2), 319–323 (2005).

H. Y. Park, H. J. Kim, M. Jung, C. H. Chung, R. Hasham, C. S. Park, and E. H. Choi, “A long-standing hyperglycaemic condition impairs skin barrier by accelerating skin ageing process,” Experimental Dermatology 20(12), 969–974 (2011).

S. Sakai, Y. Endo, N. Ozawa, T. Sugawara, A. Kusaka, T. Sayo, H. Tagami, and S. Inoue, “Characteristics of the epidermis and stratum corneum of hairless mice with experimentally induced diabetes mellitus,” Journal of Investigative Dermatology 120(1), 79–85 (2003).

K. R. Taylor, A. E. Costanzo, and J. M. Jameson, “Dysfunctional γδ T cells contribute to impaired keratinocyte homeostasis in mouse models of obesity,” Journal of Investigative Dermatology 131(12), 2409–2418 (2011).

P. Zakharov, M. S. Talary, I. Kolm, and A. Caduff, “Full-field optical coherence tomography for the rapid estimation of epidermal thickness: study of patients with diabetes mellitus type 1,” Physiological Measurement 31(2), 193–205 (2010).

X. Chen, W. Lin, S. Lu, T. Xie, G. Kui, Y. Shi, J. Zou, Z. Liu, and W. Liao, “Mechanisitic study of endogenous skin lesions in diabetic rats,” Experimental Dermatology 19(12), 1088–1095 (2010).

U. Bertheim, A. Engstorm-Laurent, P. Hofer, P. Hallgren, J. Asplund, and S. Hellstrom, “Loss of hyaluronan in the basement membrane zone of the skin correlates to the degree of stiff hands in diabetic patients,” Acta Dermato-Venereologica 82(5), 329–334 (2002).

J. G. B. Derraik, M. Rademaker, W. S. Cutfield, T. E. Pinto, S. Tregurtha, A. Faherty, J. M. Peart, P. L. Drury, and P. L. Hofman, “Effects of Age, Gender, BMI, and Anatomical Site on Skin Thickness in Children and Adults with Diabetes,” PLoS ONE 9(1), e86637 (2014).

A. A. Tahrani, W. Zeng, J. Sakher, M. K. Piya, S. Hughes, K. Dubb, and M. J. Stevens, “Cutaneous structural and biochemical correlates of foot complications in high-risk diabetes,” Diabetes Care 35(9), 1913–1918 (2012).

N. C. Avery, A. J. Bailey, “The effects of the Maillard reaction on the physical properties and cell interactions of collagen,” Pathologie Biologie 54(7), 387–395 (2006).

A. J. Argyropoulos, P. Robichaud, R. M. Balimunkwe, G. J. Fisher, C. Hammerberg, Y. Yan, and T. Quan, “Alterations of Dermal Connective Tissue Collagen in Diabetes: Molecular Basis of Aged-Appearing Skin,” PLoS ONE 11(4), e0153806 (2016).

L. V. Wang (Ed.), Photoacoustic Imaging and Spectroscopy, CRC Press (2009).