Abstract
Purpose
To determine whether there are significant correlations between the hemodynamics of the optic nerve head (ONH) and choroid as shown by laser speckle flowgraphy (LSFG) and the fasting blood sugar (FBS) and HbA1c level in patients with/without diabetes mellitus (DM).
Methods
We analyzed 196 consecutive patients (151 men, 45 women). The pulse waveform analysis parameters of the mean blur rate (MBR), blowout score (BOS) and blowout time (BOT) in the ONH and choroid were evaluated. We used a multiple regression analysis to determine the independent factors for the LSFG parameters that are significantly correlated with FBS or HbA1c. We evaluated the relationship between the LSFG parameters FBS and HbA1c obtained from the 147 non-DM patients.
Results
The multiple regression analysis revealed that hematocrit and HbA1c were factors contributing independently to the choroid MBR. The age, gender, pulse pressure, heart rate, spherical refraction and HbA1c were identified as factors contributing independently to the BOS in the ONH. The multiple regression analysis indicated that age, height, pulse pressure, heart rate and HbA1c were factors contributing independently to the BOS in the choroid. A Pearson’s correlation analysis showed that the BOT values in the ONH and choroid were significantly correlated with the HbA1c in the non-DM patients.
Conclusion
Our results confirmed that HbA1c, even within the normal range, affected the blood flow in the ONH and choroid. LSFG may be a useful method to detect abnormalities of asymptomatic ocular circulation.
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References
Taylor HR, Keeffe JE (2001) World blindness a 21st century perspective. Br J Ophthalmol 85:261–266
Aeillo LP, Gardner TW, King GL, Blankenship G, Cavallerano JD, Ferris FL 3rd, Klein R (1998) Diabetic retinopathy. Diabetes Care 21:143–156
Aiello LP, Avery RL, Arrigg PG, Keyt BA, Jampel HD, Shah ST, Pasquale LR, Thieme H, Iwamoto MA, Park JE, Nguyen HV, Ailleo LM, Ferrara N, King GL (1994) Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N Engl J Med 331:1480–1487
McLeod DS, Lefer DJ, Merges C, Lutty GA (1995) Enhanced expression of intracellular adhesion molecule-1 and P-selectin in the diabetic human retina and choroid. Am J Pathol 147:642–653
Ishida S, Yamashiro K, Usui T, Kaji Y, Ogura Y, Hida T, Honda Y, Oguchi Y, Adamis AP (2003) Leukocytes mediate retinal vascular remodeling during development and vasoobliteration in disease. Nat Med 9:781–788
Stitt AW (2003) The role of advanced glycation in pathogenesis of diabetic retinopathy. Exp Mol Pathol 75:95–108
Ishii H, Koya D, King GL (1998) Protein kinase C activation and its role in the development of vascular complication in diabetes mellitus. J Mol Med 76:21–31
Nishikawa T, Edelstein D, Du X, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, Giardino I, Brownlee M (2000) Normalizing mitochondrial superoxide production blocks three pathways of hyperglycemic damage. Nature 404:787–790
Ceriello A (2003) New insights on oxidative stress and diabetic complications may lead to a “causal” antioxidant therapy. Diabetes Care 26:1589–1596
Tamaki Y, Araie M, Kawamoto E, Eguchi S, Fujii H (1995) Non-contact, two-dimensional measurement of tissue circulation in choroid and optic nerve head using laser speckle phenomenon. Exp Eye Res 60:373–383
Isono H, Kishi S, Kimura Y, Hagiwara N, Konishi N, Fujii H (2003) Observation of choroidal circulation using index of erythrocytic velocity. Arch Ophthalmol 121:225–231
Fujii H (1994) Visualisation of retinal blood flow by laser speckle flow-graphy. Med Biol Eng Comput 32:302–304
Fujii H (2000) Laser speckle flowgraphy. In medical diagnostic techniques and procedures. Narosa Publishing House, New Delhi, pp 216–224
Takahashi H, Sugiyama T, Tokushige H, Maeno T, Nakazawa T, Ikeda T, Araie M (2013) Comparison of CCD-equipped laser speckle flowgraphy with hydrogen gas clearance method in the measurement of optic nerve head microcirculation in rabbits. Exp Eye Res 108:10–15
Sugiyama T (2014) Basic technology and clinical applications of the updated model of laser speckle flowgraphy to ocular diseases. Photonics 1:220–234
Shiba T, Takahashi M, Hori Y, Maeno T (2012) Pulse-wave analysis of optic nerve head circulation is significantly correlated with brachial–ankle pulse-wave velocity, carotid intima–media thickness, and age. Graefes Arch Clin Exp Ophthalmol 250:1275–1281
Shiba T, Takahashi M, Hori Y, Maeno T, Shirai K (2012) Optic nerve head circulation determined by pulse wave analysis is significantly correlated with cardio ankle vascular index, left ventricular diastolic function, and age. J Atheroscler Thromb 19:999–1005
Rina M, Shiba T, Takahashi M, Hori Y, Maeno T (2015) Pulse waveform analysis of optic nerve head circulation for predicting carotid atherosclerotic changes. Graefes Arch Clin Exp Ophthalmol 253:2285–2291
Sugiyama T, Araie M, Riva CE, Schmetterer L, Orgul S (2010) Use of laser speckle flowgraphy in ocular blood flow research. Acta Ophthalmol 88:723–729
Menke A, Casagrande S, Geiss L, Cowie CC (2015) Prevalence of and trends in diabetes among adults in the United States, 1988–2012. JAMA 314:1021–1029
Yanagida K, Iwase T, Yamamoto K, Ra E, Kaneko H, Murotani K, Matsui S, Terasaki H (2015) Sex-related differences in ocular blood flow of healthy subjects using laser speckle flowgraphy. Invest Ophthalmol Vis Sci 56:4880–4890
Kunikata H, Aizawa N, Kudo M, Mugikura S, Nitta F, Morimoto R, Iwakura Y, Ono Y, Satoh F, Takahashi H, Ito S, Takahashi S, Nakazawa T (2015) Relationship of ocular microcirculation, measured by laser speckle flowgraphy, and silent brain infarction in primary aldosteronism. PLoS One 10:e0117452
Tsuda S, Kunikata H, Shimura M, Aizawa N, Omodaka K, Shiga Y, Yasuda M, Yokoyama Y, Nakazawa T (2014) Pulse-waveform analysis of normal population using laser speckle flowgraphy. Curr Eye Res 39:1207–1215
Shiba T, Takahashi M, Maeno T (2014) Pulse-wave analysis of optic nerve head circulation is significantly correlated with kidney function in patients with and without chronic kidney disease. J Ophthalmol 291687
Langham ME, Farrell RA, O’Brien V, Silver DM, Schilder P (1989) Blood flow in the human eye. Acta Ophthalmol 67:9–13
Geyer O, Neudorfer M, Snir T, Goldstein M, Rock T, Silver DM, Bartov E (1999) Pulsatile ocular blood flow in diabetic retinopathy. Acta Ophthalmol Scand 77:522–552
MacKinnon JR, O’Brien C, Swa K, Aspinall P, Butt Z, Cameron D (1997) Pulsatile ocular blood flow in untreated diabetic retinopathy. Acta Ophthalmol Scand 75:661–664
Nagaoka T, Kitaya N, Sugawara R, Yokota H, Mori F, Hikichi T, Fujio N, Yoshida A (2004) Alteration of choroidal circulation in the foveal region in patients with type 2 diabetes. Br J Ophthalmol 88:1060–1063
Dimitrova G, Kato S, Tamaki Y, Yamashita H, Nagahara M, Sakurai M, Kitano S, Fukushima H (2001) Choroidal circulation in diabetic patients. Eye (Lond) 15:602–607
MacKinnon JR, McKillop G, O’Brien C, Swa K, Butt Z, Nelson P (2000) Colour Doppler imaging of the ocular circulation in diabetic retinopathy. Acta Ophthalmol Scand 78:386–389
Nagaoka T, Sato E, Takahashi A, Yokota H, Sogawa K, Yoshida A (2010) Impaired retinal circulation in patients with type 2 diabetes mellitus: retinal laser Doppler velocimetry study. Invest Ophthalmol Vis Sci 51:6729–6734
Perrott RL, North RV, Drasdo N, Ahmed KA, Owens DR (2001) The influence of plasma glucose upon pulsatile ocular blood flow in subjects with type II diabetes mellitus. Diabetologia 44:700–705
Polak K, Dallinger S, Polska E, Findl O, Eichler HG, Wolzt M, Schmetterer L (2000) Effects of insulin on retinal and pulsatile choroidal blood flow in humans. Arch Ophthalmol 118:55–59
Verdoia M, Schaffer A, Cassetti E, Barbieri L, Di Ruocco MV, Perrone-Filardi P, Marino P, De Luca G, Novara Atherosclerosis Study Group (NAS) (2014) Glycosylated hemoglobin and coronary artery disease in patients without diabetes mellitus. Am J Prev Med 47:9–16
Mukai N, Ninomiya T, Hata J, Hirakawa Y, Ikeda F, Fukuhara M, Hotta T, Koga M, Nakamura U, Kang D, Kitazono T, Kiyohara Y (2015) Association of hemoglobin A1c and glycated albumin with carotid atherosclerosis in community-dwelling Japanese subjects: the Hisayama Study. Cardiovasc Diabetol. doi:10.1186/s12933-015-0247-7
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Shiba, C., Shiba, T., Takahashi, M. et al. Relationship between glycosylated hemoglobin A1c and ocular circulation by laser speckle flowgraphy in patients with/without diabetes mellitus. Graefes Arch Clin Exp Ophthalmol 254, 1801–1809 (2016). https://doi.org/10.1007/s00417-016-3437-4
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DOI: https://doi.org/10.1007/s00417-016-3437-4