Serum adiponectin levels in obese type 2 diabetic patients with diabetic retinopathy
DOI:
https://doi.org/10.31288/oftalmolzh201753944Keywords:
diabetic retinopathy, type 2 diabetes mellitus, obesity, adiponectinAbstract
Background. Diabetic retinopathy (DR) is one of the main complications of diabetes mellitus, the main cause of irreversible blindness in patients of working age in industrialized countries, has a high incidence rates and refers to neovascular eye diseases. At the present time, additional factors that affect the sensitivity to chronic hyperglycemia, the formation of microvascular complications, in particular, DR, include obesity and obesity-associated hormones of adipose tissue (adipokines: leptin, adiponectin, resistin, etc.).
Purpose. To investigate the serum adiponectin levels in patients at different stages of DR in type 2 diabetes mellitus (T2DM) and obesity.
Material and Methods. Study involved 99 patients, divided into 2 groups. The 1-st group (control group) consisted of 23 persons with obesity without T2DM (both male and female subjects; mean age, 57.03 ± 4.91 years), the 2-nd group consisted of 76 patients with T2DM, obesity and DR (both male and female subjects; mean age, 59.98 ± 4.17 years; mean duration of diabetes, 10.01 ± 2.81 years; mean glycated hemoglobin (HbA1C) level, 10.94 ± 2.08%), subdivided into 3 subgroups: with minimal and mild non-proliferative DR, with moderate to severe non-proliferative DR, with proliferative DR. The concentration of serum adiponectin was determined by ELISA kit. Statistical analysis included one- and two-factor analysis of variance.
Results. Patients with mild non-proliferative DR had somewhat lower (worst) adiponectin levels among patients aged 60 and below with DM subcompensation. The lowest serum adiponectin levels were common for moderate to severe non-proliferative DR among T2DM patients aged above 60 with duration of diabetes of 10 years or less and with T2DM compensation. Among T2DM patients with proliferative DR, the worst serum adiponectin levels were common for T2DM patients aged 60 and below with duration of diabetes of less than 10 years and with T2DM compensation. Considering statistic values of serum adiponectin levels for this stage, it should be noted that, for conditionally combined proliferative DR with severe and moderate DR, statistically significant changes (р=0.007) consisted in the decreased serum adiponectin levels in T2DM compensation.
Conclusions. Minimal and mild non-proliferative DR is characterized by a significant lower serum adiponectin level compared with the subsequent stages in subcompensation of T2DM.
References
1.Adamczak M, Wiecek A, Funahashi T, Chudek J, Kokot F, Matsuzawa Y. Decreased plasma adiponectin concentration in patients with essential hypertension. American Journal of Hypertension. 2003; 16: 72-5.https://doi.org/10.1016/S0895-7061(02)03197-7
2.Aiello LM. Perspectives on diabetic retinopathy. American Journal of Ophthalmology. 2003; 136: 122-35.https://doi.org/10.1016/S0002-9394(03)00219-8
3.AntonopoulosAS, MargaritisM, CoutinhoP, et al. Adiponectin as a link between type 2 diabetes and vascular NADPH oxidase activity in the human arterial wall: the regulatory role of perivascular adipose tissue. Diabetes.2015; 64: 2207-19.https://doi.org/10.2337/db14-1011
4.Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y. Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochemical and Biophysical Research Communications. 1999; 257: 79-83.https://doi.org/10.1006/bbrc.1999.0255
5.Be?towski J. Adiponectin and resistin - new hormones of white adipose tissue. Medical Science Monitor. 2003; 9: RA55-61.
6.Berg AH, Combs TP, Scherer PE. ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Metab. 2002;13:84-9.https://doi.org/10.1016/S1043-2760(01)00524-0
7.Diabetes Control and Complications Trial Research Group, Clustering of long-term complications in families with diabetes in the Diabetes Control and Complications Trial. Diabetes. 1997; 46: 1829-39.https://doi.org/10.2337/diab.46.11.1829
8.D?ez JJ, Iglesias P. The role of the novel adipocyte-derived hormone adiponectin in human disease. Eur J Endocrinol. 2003; 148: 293-300.https://doi.org/10.1530/eje.0.1480293
9.Fernandez-Real JM, Botas-Cervero P, Lopez-Bermano A, Casamitjana R, Funahashi T, Delgado E, Kihara S, RicartW. Adiponectin is independently associated with glycosylated haemoglobin. European Journal of Endocrinology. 2012; 150: 201-5.https://doi.org/10.1530/eje.0.1500201
10.Gariano RF, Gardner TW. Retinal angiogenesis in development and disease. Nature. 2005; 438: 960-6.https://doi.org/10.1038/nature04482
11.Hadjadj S, Aubert R, Fumeron F, et al. Increased plasma adiponectin concentrations are associated with microangiopathy in type 1 diabetic subjects. Diabetologia. 2005; 48: 1088-92.https://doi.org/10.1007/s00125-005-1747-x
12.Hotta K, Funahashi T, Arita Y, Takahashi M, Matsuda M, Okamoto Y, Iwahashi H, Kuriyama H, Ouchi N, Maeda K, NishidaM, Kihara S, Sakai N, Nakajima T, Hasegawa K, Muraguchi M, Ohmoto Y, Nakamura T, Yamashita S, Hanafusa T, Matsuzawa Y. Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arteriosclerosis, Thrombosis, and Vascular Biology. 2000; 20: 1595-99.https://doi.org/10.1161/01.ATV.20.6.1595
13.International Diabetes Federation.Managing older people with Type 2 Diabetes. Global Guideline.2013.
14.Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin Epidemiologic Study: II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Archives of Ophthalmology. 1984; 102: 520-6.https://doi.org/10.1001/archopht.1984.01040030398010
15.Kumada M, Kihara S, Sumitsuji S, et al. Association of hypoadiponectinemia with coronary artery disease in men. Arterioscler Thromb Vasc Biol. 2003; 23: 85-9.https://doi.org/10.1161/01.ATV.0000048856.22331.50
16.Kuo Jane Z, Guo Xiuqing, Klein Ronald, Klein Barbara E, Genter Pauline, Roll Kathryn, Yang Hai, Goodarzi Mark O, Rotter Jerome I, Chen Yii-Der Ida, Ipp Eli. Adiponectin, Insulin Sensitivity and Diabetic Retinopathy in Latinos With Type 2 Diabetes. JCEM. 2015; 100(9): 3348-55.https://doi.org/10.1210/jc.2015-1221
17.Kuo JZ, Guo X, Klein R, et al. Systemic soluble tumor necrosis factor receptors 1 and 2 are associated with severity of diabetic retinopathy in Hispanics. Ophthalmology. 2012; 119: 1041-46.https://doi.org/10.1016/j.ophtha.2011.10.040
18.Leslie RD, Pozzilli P. An introduction to new advances in diabetes. DiabetesMetabolism Research and Reviews. 2002; 18Suppl 1: S1-S6.https://doi.org/10.1002/dmrr.203
19.LianK, DuC, LiuY, ZhuD, YanW, ZhangH, HongZ, LiuP, ZhangL, PeiH, ZhangJ, GaoC, XinC, ChengH, XiongL, TaoL.Impaired adiponectin signaling contributes to disturbed catabolism of branched-chai n amino acids in diabetic mice. Diabetes. 2015; 64: 49-59.https://doi.org/10.2337/db14-0312
20.Lindsay RS, Funahashi T, Hanson RL, et al. Adiponectin and development of type 2 diabetes in the Pima Indian population. Lancet. 2002; 360: 57-8.https://doi.org/10.1016/S0140-6736(02)09335-2
21.Maeda N, Shimomura I, Kishida K, Nishizawa H, Matsuda M, Nagaretani H, Furuyama N, Kondo H, Takahashi M, Arita Y, Komuro R, Ouchi N, Kihara S, Tochino Y, Okutomi K, Horie M, Takeda S, Aoyama T, Funahashi T, Matsuzawa Y. Diet-induced insulin resistance in mice lacking adiponectin/ACRP30. Nature Medicine. 2002; 8: 731-7.https://doi.org/10.1038/nm724
22.Maeda K, Okubo K, Shimomura I, Funahashi T, Matsuzawa Y, Matsubara K. cDNA cloning and expression of a novel adipose specific collagen-like factor, apM1 (AdiPose Most Abundant Gene Transcript 1). Biochemical and Biophysical Research Communications. 1996; 221: 286-9.https://doi.org/10.1006/bbrc.1996.0587
23.Malachkova N. V., Komarovskaya I. V., Kyryliuk M. L. Uroven' glikemii i insulinorezistentnosti u bol'nyh s diabeticheskoj retinopatiej, saharnym diabetom 2-go tipa i ozhireniem[Blood glucose level and insulin resistance in patients with type 2 diabetic mellitus, diabetic retinopathy and obesity]. Mezhdunarodnyi Endokrinologicheskii Zhurnal (IEJ). 2017; 3(13): 27-32. (In Russian) https://doi.org/10.22141/2224-0721.13.3.2017.104108
24.Matsuda M, Kawasaki F, Yamada K, et al. Impact of adiposity and plasma adipocytokines on diabetic angiopathies in Japanese Type 2 diabetic subjects. Diabet Med.2004;21:881-8.https://doi.org/10.1111/j.1464-5491.2004.01261.x
25.Ouchi N, Ohishi M, Kihara S, Funahashi T, Nakamura T, Nagaretani H, Kumada M, Ohashi K, Okamoto Y, Nishizawa H, Kishida K, Maeda N, Nagasawa A, Kobayashi H, Hiraoka H, Komai N, Kaibe M, Rakugi H, Ogihara T, Matsuzawa Y. Association of hypoadiponectinemia with impaired vasoreactivity. Hypertension. 2003; 42: 231-4.https://doi.org/10.1161/01.HYP.0000083488.67550.B8
26.Ouchi N, Kihara S, Arita Y, Nishida M, Matsuyama A, Okamoto Y, Ishigami M, Kuriyama H, Kishida K, Nishizawa H, Hotta K, Muraguchi M, Ohmoto Y, Yamashita S, Funahashi T, Matsuzawa Y. Adipocyte-derived plasma protein, adiponectin, suppresses lipid accumulation and class A scavenger receptor expression in human monocyte-derived macrophages. Circulation. 2001; 103: 1057-63.https://doi.org/10.1161/01.CIR.103.8.1057
27.Ouchi N, Kihara S, Arita Y, Maeda K, Kuriyama H, Okamoto Y, Hotta K, Nishida M, Takahashi M, Nakamura T, Yamashita S, Funahashi T, Matsuzawa Y. Novel modulator for endothelial adhesion molecules: adipocyte-derived plasma protein adiponectin. Circulation. 1999; 100: 2473-76.https://doi.org/10.1161/01.CIR.100.25.2473
28.Parker-DuffenL, NakamuraK, SilverM, Zuria gaMA, MacLauchlanS, AprahamianTR, WalshK. Divergent roles for adiponectin receptor 1 (AdipoR1) and AdipoR2 in mediating revascularization and metabolic dysfunction in vivo. J. Biol. Chem. 2014; 289: 16200-13.https://doi.org/10.1074/jbc.M114.548115
29.Sheetz MJ, King GL. Molecular understanding of hyperglycemia's adverse effects for diabetic complications. JAMA. 2002; 288: 2579-2588.https://doi.org/10.1001/jama.288.20.2579
30.Spranger J, Pfeiffer AF. New concepts in pathogenesis and treatment of diabetic retinopathy. Exp Clin Endocrinol Diabetes. 2001; 109 Suppl 2: S438-S450.https://doi.org/10.1055/s-2001-18601
31.Stefan N, Stumvoll M. Adiponectin-its role in metabolism and beyond. Horm Metab Res. 2002; 34: 469-74.https://doi.org/10.1055/s-2002-34785
32.Tielsch JM, Sommer A, Witt K, Katz J, Royall RM. Blindness and visual impairment in an American urban population. The Baltimore Eye Survey. Archives of Ophthalmology. 1990; 108: 286-290.https://doi.org/10.1001/archopht.1990.01070040138048
33.Ukkola O, Santaniemi M. Adiponectin: a link between excess adiposity and associated comorbidities? J Mol Med. 2002; 80: 696-702.https://doi.org/10.1007/s00109-002-0378-7
34.UK Prospective Diabetes Study Group Tight blood pressure control and risk of macrovascular and microvascular complications in type 2 diabetes: UKPDS 38. British Medical Journal. 1998; 317: 703-13.https://doi.org/10.1136/bmj.317.7160.703
35.Vionnet N, Hani El-H, Dupont S, Gallina S, Francke S, Dotte S, De Matos F, Durand E, Lepretre F, Lecoeur C, Gallina P, Zekiri L, Dina C, Froguel P. Genome wide search for type 2 diabetes-susceptibility genes in French whites: evidence for a novel susceptibility locus for early-onset diabetes on chromosome 3q2-qter and independent replication of a type diabetes locus on chromosome 1q2-q24. American Journal of Human Genetics. 2000; 67: 1470-80.https://doi.org/10.1086/316887
36.Ye R, Scherer PE. Adiponectin, driver or passenger on the road to insulin sensitivity? Mol Metab. 2013; 2: 133-141.https://doi.org/10.1016/j.molmet.2013.04.001
37.Zietz B, Buechler C, Kobuch K, Neumeier M, Sch?lmerich J, Sch?fler A. Serum levels of adiponectin are associated with diabetic retinopathy and with adiponectin gene mutations in Caucasian patients with diabetes mellitus type 2. Exp Clin Endocrinol Diabetes. 2008; 116: 532-6.https://doi.org/10.1055/s-2008-1058086
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