Association Between Insulin Resistance and Cardinal Rheological Parameters in Young Healthy Japanese Individuals During 75g Oral Glucose Tolerance Test

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Abstract

Background: Insulin resistance is a well-known predictor and risk factor for type 2 diabetes mellitus (T2DM). Higher hematocrit induced by higher insulin resistance affects blood rheology.

Objective: This study intended to reveal the association between indices of insulin resistance and hemorheological parameters during a 75 g oral glucose tolerance test (75-g OGTT).

Methods: A total of 575 healthy young Japanese participants took 75-g OGTT. We then analyzed the association between insulin resistance indices and hematological parameters.

Results: The Homeostasis Model Assessment of Insulin Resistance (HOMA-IR) was significantly correlated with hematocrit (Ht), hemoglobin (Hb), red blood cell (RBC), white blood cell (WBC), platelet count, lipid parameters and body mass index (BMI). The Matsuda index was negatively correlated with RBC count, WBC count, platelet count, total cholesterol (TC), low-density lipoprotein- cholesterol (LDL-C), triglyceride (TG), and positively correlated with high-density lipoprotein- cholesterol (HDL-C). The disposition index was negatively correlated with Hb, RBC count, LDL-C and BMI, and positively correlated with HDL-C. The Homeostasis Model Assessment of beta cell (HOMA-β) was positively correlated with WBC count, platelet count, TC, LDL-C and TG. The insulinogenic index was positively correlated with WBC count, platelet count and TC. Multiple regression analysis revealed that HOMA-IR was independently associated with TG, and the Matsuda index was independently associated with TG, WBC count, and platelet count. The insulinogenic index was independently associated with WBC count.

Conclusion: Cardinal rheological parameters reflected insulin resistance and release even in young healthy Japanese individuals within the physiological range of glycemic control.

Keywords: OGTT, Insulin secretion, insulin resistance, RBC count, WBC count, platelet count, blood rheology.

Graphical Abstract

[1]
Diabetes around the world in 2021. IDF Diabetes Atlas. Available from: https://www.diabetesatlas.org/en/ (Accessed on February 12, 2021).
[2]
Weiss, R.; Dziura, J.; Burgert, T.S.; Tamborlane, W.V.; Taksali, S.E.; Yeckel, C.W.; Allen, K.; Lopes, M.; Savoye, M.; Morrison, J.; Sherwin, R.S.; Caprio, S. Obesity and the metabolic syndrome in children and adolescents. N. Engl. J. Med., 2004, 350(23), 2362-2374.
[http://dx.doi.org/10.1056/NEJMoa031049] [PMID: 15175438]
[3]
Ogden, C.L.; Carroll, M.D.; Flegal, K.M. High body mass index for age among US children and adolescents, 2003-2006. JAMA, 2008, 299(20), 2401-2405.
[http://dx.doi.org/10.1001/jama.299.20.2401] [PMID: 18505949]
[4]
Ahluwalia, N.; Dalmasso, P.; Rasmussen, M.; Lipsky, L.; Currie, C.; Haug, E.; Kelly, C.; Damsgaard, M.T.; Due, P.; Tabak, I.; Ercan, O.; Maes, L.; Aasvee, K.; Cavallo, F. Trends in overweight prevalence among 11-, 13- and 15-year-olds in 25 countries in Europe, Canada and USA from 2002 to 2010. Eur. J. Public Health, 2015, 25(Suppl. 2), 28-32.
[http://dx.doi.org/10.1093/eurpub/ckv016] [PMID: 25805783]
[5]
Chiarelli, F.; Marcovecchio, M.L. Insulin resistance and obesity in childhood. Eur. J. Endocrinol., 2008, 159(Suppl. 1), S67-S74.
[http://dx.doi.org/10.1530/EJE-08-0245] [PMID: 18805916]
[6]
Cruz, M.L.; Shaibi, G.Q.; Weigensberg, M.J.; Spruijt-Metz, D.; Ball, G.D.; Goran, M.I. Pediatric obesity and insulin resistance: Chronic disease risk and implications for treatment and prevention beyond body weight modification. Annu. Rev. Nutr., 2005, 25, 435-468.
[http://dx.doi.org/10.1146/annurev.nutr.25.050304.092625] [PMID: 16011474]
[7]
Lee, J.M. Insulin resistance in children and adolescents. Rev. Endocr. Metab. Disord., 2006, 7(3), 141-147.
[http://dx.doi.org/10.1007/s11154-006-9019-8] [PMID: 17165145]
[8]
Pankow, J.S.; Jacobs, D.R., Jr; Steinberger, J.; Moran, A.; Sinaiko, A.R. Insulin resistance and cardiovascular disease risk factors in children of parents with the insulin resistance (metabolic) syndrome. Diabetes Care, 2004, 27(3), 775-780.
[http://dx.doi.org/10.2337/diacare.27.3.775] [PMID: 14988301]
[9]
Shanik, M.H.; Xu, Y.; Škrha, J.; Dankner, R.; Zick, Y.; Roth, J. Insulin resistance and hyperinsulinemia: Is hyperinsulinemia the cart or the horse? Diabetes Care, 2008, 31(Suppl. 2), S262-S268.
[http://dx.doi.org/10.2337/dc08-s264] [PMID: 18227495]
[10]
Allan, C.L.; Flett, B.; Dean, H.J. Quality of life in first nation youth with type 2 diabetes. Matern. Child Health J., 2008, 12(Suppl. 1), 103-109.
[http://dx.doi.org/10.1007/s10995-008-0365-x] [PMID: 18500548]
[11]
Hood, K.K.; Beavers, D.P.; Yi-Frazier, J.; Bell, R.; Dabelea, D.; Mckeown, R.E.; Lawrence, J.M. Psychosocial burden and glycemic control during the first 6 years of diabetes: Results from the SEARCH for diabetes in youth study. J. Adolesc. Health, 2014, 55(4), 498-504.
[http://dx.doi.org/10.1016/j.jadohealth.2014.03.011] [PMID: 24815959]
[12]
Icks, A.; Rosenbauer, J.; Rathmann, W.; Haastert, B.; Gandjour, A.; Giani, G. Direct costs of care in germany for children and adolescents with diabetes mellitus in the early course after onset. J. Pediatr. Endocrinol. Metab., 2004, 17(11), 1551-1559.
[http://dx.doi.org/10.1515/JPEM.2004.17.11.1551] [PMID: 15570993]
[13]
Wang, G.; Dietz, W.H. Economic burden of obesity in youths aged 6 to 17 years: 1979-1999. Pediatrics, 2002, 109(5), E81-E1.
[http://dx.doi.org/10.1542/peds.109.5.e81] [PMID: 11986487]
[14]
Ishigaki, H.; Yoshida, A.; Araki, O.; Kimura, T.; Tsunekawa, K.; Shoho, Y.; Nara, M.; Aoki, T.; Ogiwara, T.; Murakami, M. Prolonged plasma glucose elevation on oral glucose tolerance test in young healthy Japanese individuals. Endocrinol Diabetes Metab, 2019, 3, e00098. Available from: https://pubmed.ncbi.nlm.nih.gov/31922025/
[15]
Matthews, D.R.; Hosker, J.P.; Rudenski, A.S.; Naylor, B.A.; Treacher, D.F.; Turner, R.C. Homeostasis model assessment: Insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia, 1985, 28(7), 412-419.
[http://dx.doi.org/10.1007/BF00280883] [PMID: 3899825]
[16]
Matsuda, M.; DeFronzo, R.A. Insulin sensitivity indices obtained from oral glucose tolerance testing: Comparison with the euglycemic insulin clamp. Diabetes Care, 1999, 22(9), 1462-1470.
[http://dx.doi.org/10.2337/diacare.22.9.1462] [PMID: 10480510]
[17]
Kosaka, K.; Kuzuya, T.; Yoshinaga, H.; Hagura, R. A prospective study of health check examinees for the development of non-insulin-dependent diabetes mellitus: Relationship of the incidence of diabetes with the initial insulinogenic index and degree of obesity. Diabet. Med., 1996, 13(9 Suppl. 6), S120-S126.
[http://dx.doi.org/10.1002/dme.1996.13.s6.120] [PMID: 8894495]
[18]
Olshansky, S.J.; Passaro, D.J.; Hershow, R.C.; Layden, J.; Carnes, B.A.; Brody, J.; Hayflick, L.; Butler, R.N.; Allison, D.B.; Ludwig, D.S. A potential decline in life expectancy in the United States in the 21st century. N. Engl. J. Med., 2005, 352(11), 1138-1145.
[http://dx.doi.org/10.1056/NEJMsr043743] [PMID: 15784668]
[19]
Poyrazoglu, S.; Bas, F.; Darendeliler, F. Metabolic syndrome in young people. Curr. Opin. Endocrinol. Diabetes Obes., 2014, 21(1), 56-63.
[http://dx.doi.org/10.1097/01.med.0000436414.90240.2c] [PMID: 24247648]
[20]
Rask-Madsen, C.; Kahn, C.R. Tissue-specific insulin signaling, metabolic syndrome, and cardiovascular disease. Arterioscler. Thromb. Vasc. Biol., 2012, 32(9), 2052-2059.
[http://dx.doi.org/10.1161/ATVBAHA.111.241919] [PMID: 22895666]
[21]
Reaven, G.M. The metabolic syndrome: Time to get off the merry-go-round? J. Intern. Med., 2011, 269(2), 127-136.
[http://dx.doi.org/10.1111/j.1365-2796.2010.02325.x] [PMID: 21129047]
[22]
Letcher, R.L.; Chien, S.; Pickering, T.G.; Laragh, J.H. Elevated blood viscosity in patients with borderline essential hypertension. Hypertension, 1983, 5(5), 757-762.
[http://dx.doi.org/10.1161/01.HYP.5.5.757] [PMID: 6352482]
[23]
Seplowitz, A.H.; Chien, S.; Smith, F.R. Effects of lipoproteins on plasma viscosity. Atherosclerosis, 1981, 38(1-2), 89-95.
[http://dx.doi.org/10.1016/0021-9150(81)90107-6] [PMID: 7470209]
[24]
Matsuo, K.; Ueda, Y.; Nishio, M.; Hirata, A.; Asai, M.; Nemoto, T.; Kashiwase, K.; Kodama, K. Thrombogenic potential of whole blood is higher in patients with acute coronary syndrome than in patients with stable coronary diseases. Thromb. Res., 2011, 128(3), 268-273.
[http://dx.doi.org/10.1016/j.thromres.2011.04.001] [PMID: 21531446]
[25]
Tzoulaki, I.; Murray, G.D.; Lee, A.J.; Rumley, A.; Lowe, G.D.; Fowkes, F.G. Relative value of inflammatory, hemostatic, and rheological factors for incident myocardial infarction and stroke: The edinburgh artery study. Circulation, 2007, 115(16), 2119-2127.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.106.635029] [PMID: 17404162]
[26]
Hanley, A.J.; Retnakaran, R.; Qi, Y.; Gerstein, H.C.; Perkins, B.; Raboud, J.; Harris, S.B.; Zinman, B. Association of hematological parameters with insulin resistance and beta-cell dysfunction in nondiabetic subjects. J. Clin. Endocrinol. Metab., 2009, 94(10), 3824-3832.
[http://dx.doi.org/10.1210/jc.2009-0719] [PMID: 19622625]
[27]
Medalie, J.H.; Papier, C.M.; Goldbourt, U.; Herman, J.B. Major factors in the development of diabetes mellitus in 10,000 men. Arch. Intern. Med., 1975, 135(6), 811-817.
[http://dx.doi.org/10.1001/archinte.1975.00330060055007] [PMID: 1130926]
[28]
Salazar, M.R.; Carbajal, H.A.; Espeche, W.G.; Dulbecco, C.A.; Aizpurúa, M.; Marillet, A.G.; Echeverría, R.F.; Reaven, G.M. Relationships among insulin resistance, obesity, diagnosis of the metabolic syndrome and cardio-metabolic risk. Diab. Vasc. Dis. Res., 2011, 8(2), 109-116.
[http://dx.doi.org/10.1177/1479164111403170] [PMID: 21562062]
[29]
Simmonds, M.J.; Meiselman, H.J.; Baskurt, O.K. Blood rheology and aging. J. Geriatr. Cardiol., 2013, 10(3), 291-301.
[PMID: 24133519]
[30]
Moan, A.; Nordby, G.; Os, I.; Birkeland, K.I.; Kjeldsen, S.E. Relationship between hemorrheologic factors and insulin sensitivity in healthy young men. Metabolism, 1994, 43(4), 423-427.
[http://dx.doi.org/10.1016/0026-0495(94)90070-1] [PMID: 8159097]
[31]
Yoshida, K.; Kimura, T.; Aoki, T.; Tsunekawa, K.; Araki, O.; Shoho, Y.; Nara, M.; Sumino, H.; Murakami, M. Fasting serum insulin levels and insulin resistance are associated with blood rheology in Japanese young adults without diabetes. J. Int. Med. Res., 2016, 44(3), 496-507.
[http://dx.doi.org/10.1177/0300060515627561] [PMID: 26920928]
[32]
Vasques, A.C.J.; Rosado, L.E.; Cássia GAlfenas, Rd.; Geloneze, B. [Critical analysis on the use of the homeostasis model assessment (HOMA) indexes in the evaluation of the insulin resistance and the pancreatic beta cells functional capacity]. Arq. Bras. Endocrinol. Metabol, 2008, 52(1), 32-39.
[http://dx.doi.org/10.1590/S0004-27302008000100006] [PMID: 18345394]
[33]
van der Aa, M.P.; Knibbe, C.A.; Boer, A.; van der Vorst, M.M. Definition of insulin resistance affects prevalence rate in pediatric patients: A systematic review and call for consensus. J. Pediatr. Endocrinol. Metab., 2017, 30(2), 123-131.
[http://dx.doi.org/10.1515/jpem-2016-0242] [PMID: 27984205]
[34]
Weiss, R.; Taksali, S.E.; Tamborlane, W.V.; Burgert, T.S.; Savoye, M.; Caprio, S. Predictors of changes in glucose tolerance status in obese youth. Diabetes Care, 2005, 28(4), 902-909.
[http://dx.doi.org/10.2337/diacare.28.4.902] [PMID: 15793193]
[35]
Sumino, H.; Nara, M.; Seki, K.; Takahashi, T.; Kanda, T.; Ichikawa, S.; Goto-Onozato, K.; Koya, S.; Murakami, M.; Kurabayashi, M. Effect of antihypertensive therapy on blood rheology in patients with essential hypertension. J. Int. Med. Res., 2005, 33(2), 170-177.
[http://dx.doi.org/10.1177/147323000503300204] [PMID: 15790128]
[36]
Sumino, H.; Ichikawa, S.; Takahashi, T.; Sakamoto, H.; Goto-Onozato, K.; Koya, S.; Kanda, T.; Nara, M.; Seki, K.; Murakami, M.; Kurabayashi, M. Conjugated estrogen plus medroxyprogesterone does not impair blood rheological properties in hypertensive postmenopausal women. Maturitas, 2006, 53(3), 306-314.
[http://dx.doi.org/10.1016/j.maturitas.2005.05.018] [PMID: 16040211]
[37]
Muranaka, Y.; Kunimoto, F.; Takita, J.; Sumino, H.; Nara, M.; Kuwano, H.; Murakami, M. Impaired blood rheology in critically ill patients in an intensive care unit. J. Int. Med. Res., 2006, 34(4), 419-427.
[http://dx.doi.org/10.1177/147323000603400412] [PMID: 16989499]
[38]
Seki, K.; Sumino, H.; Nara, M.; Ishiyama, N.; Nishino, M.; Murakami, M. Relationships between blood rheology and age, body mass index, blood cell count, fibrinogen, and lipids in healthy subjects. Clin. Hemorheol. Microcirc., 2006, 34(3), 401-410.
[PMID: 16614464]
[39]
Machida, T.; Sumino, H.; Fukushima, M.; Kotajima, N.; Amagai, H.; Murakami, M. Blood rheology and the low-density lipoprotein cholesterol/high-density lipoprotein cholesterol ratio in dyslipidaemic and normolipidaemic subjects. J. Int. Med. Res., 2010, 38(6), 1975-1984. Available from: https://journals.sagepub.com/doi/10.1177/147323001003800611
[http://dx.doi.org/10.1177/147323001003800611] [PMID: 21227001]
[40]
Maki, Y.; Endo, Y.; Fukushima, M.; Nishiyama, M.; Dobashi, T.; Sumino, H.; Murakami, M. Estimation of viscosity from passage time of liquids flowing through a microchannel array. J Biorheol, 2013, 26, 69-73.
[http://dx.doi.org/10.1007/s12573-012-0048-5]
[41]
Yagi, H.; Sumino, H.; Aoki, T.; Tsunekawa, K.; Araki, O.; Kimura, T.; Nara, M.; Ogiwara, T.; Murakami, M. Impaired blood rheology is associated with endothelial dysfunction in patients with coronary risk factors. Clin. Hemorheol. Microcirc., 2016, 62(2), 139-150. Available from: https://content.iospress.com/articles/clinical-hemorheology-and-microcirculation/ch1960
[http://dx.doi.org/10.3233/CH-151960] [PMID: 26444592]
[42]
Nara, M.; Sumino, H.; Nara, M.; Machida, T.; Amagai, H.; Nakajima, K.; Murakami, M. Impaired blood rheology and elevated remnant-like lipoprotein particle cholesterol in hypercholesterolaemic subjects. J. Int. Med. Res., 2009, 37(2), 308-317.
[http://dx.doi.org/10.1177/147323000903700204] [PMID: 19383223]
[43]
Barazzoni, R.; Gortan Cappellari, G.; Semolic, A.; Chendi, E.; Ius, M.; Situlin, R.; Zanetti, M.; Vinci, P.; Guarnieri, G. The association between hematological parameters and insulin resistance is modified by body mass index - results from the North-East Italy MoMa population study. PLoS One, 2014, 9(7)e101590
[http://dx.doi.org/10.1371/journal.pone.0101590] [PMID: 25000394]
[44]
Nakanishi, N.; Suzuki, K.; Tatara, K. Haematocrit and risk of development of Type 2 diabetes mellitus in middle-aged Japanese men. Diabet. Med., 2004, 21(5), 476-482.
[http://dx.doi.org/10.1111/j.1464-5491.2004.01152.x] [PMID: 15089794]
[45]
Tulloch-Reid, M.K.; Hanson, R.L.; Saremi, A.; Looker, H.C.; Williams, D.E.; Krakoff, J.; Knowler, W.C. Hematocrit and the incidence of type 2 diabetes in the pima indians. Diabetes Care, 2004, 27(9), 2245-2246.
[http://dx.doi.org/10.2337/diacare.27.9.2245] [PMID: 15333493]
[46]
Wannamethee, S.G.; Perry, I.J.; Shaper, A.G. Hematocrit and risk of NIDDM. Diabetes, 1996, 45(5), 576-579.
[http://dx.doi.org/10.2337/diab.45.5.576] [PMID: 8621006]
[47]
Wilson, P.W.; McGee, D.L.; Kannel, W.B. Obesity, very low density lipoproteins, and glucose intolerance over fourteen years: The Framingham Study. Am. J. Epidemiol., 1981, 114(5), 697-704.
[http://dx.doi.org/10.1093/oxfordjournals.aje.a113240] [PMID: 7304597]
[48]
Annerén, C.; Welsh, M.; Jansson, L. Glucose intolerance and reduced islet blood flow in transgenic mice expressing the FRK tyrosine kinase under the control of the rat insulin promoter. Am. J. Physiol. Endocrinol. Metab., 2007, 292(4), E1183-E1190.
[http://dx.doi.org/10.1152/ajpendo.00168.2006] [PMID: 17179392]
[49]
Catalano, C.; Muscelli, E.; Natali, A.; Mazzoni, A.; Masoni, A.; Bernardini, B.; Seghieri, G.; Ferrannini, E. Reciprocal association between insulin sensitivity and the haematocrit in man. Eur. J. Clin. Invest., 1997, 27(7), 634-637.
[http://dx.doi.org/10.1046/j.1365-2362.1997.1770714.x] [PMID: 9263753]
[50]
Aloulou, I.; Varlet-Marie, E.; Mercier, J.; Brun, J.F. The hemorheological aspects of the metabolic syndrome are a combination of separate effects of insulin resistance, hyperinsulinemia and adiposity. Clin. Hemorheol. Microcirc., 2006, 35(1-2), 113-119.
[PMID: 16899914]
[51]
Brun, J.F.; Varlet-Marie, E.; Raynaud de Mauverger, E.; Mercier, J. Minimal model-derived insulin sensitivity, insulin secretion and glucose tolerance: Relationships with blood rheology. Clin. Hemorheol. Microcirc., 2012, 51(1), 21-27.
[http://dx.doi.org/10.3233/CH-2011-1425] [PMID: 22240354]
[52]
Ferreira, D.; Severo, M.; Araújo, J.; Barros, H.; Guimarães, J.T.; Ramos, E. Association between insulin resistance and haematological parameters: A cohort study from adolescence to adulthood. Diabetes Metab. Res. Rev., 2019, 35(8)e3194 Available from: https://onlinelibrary.wiley.com/doi/full/10.1002/dmrr.3194
[http://dx.doi.org/10.1002/dmrr.3194] [PMID: 31206976]
[53]
Miyagawa, S.; Kobayashi, M.; Konishi, N.; Sato, T.; Ueda, K. Insulin and insulin-like growth factor I support the proliferation of erythroid progenitor cells in bone marrow through the sharing of receptors. Br. J. Haematol., 2000, 109(3), 555-562.
[http://dx.doi.org/10.1046/j.1365-2141.2000.02047.x] [PMID: 10886204]
[54]
Aoki, I.; Taniyama, M.; Toyama, K.; Homori, M.; Ishikawa, K. Stimulatory effect of human insulin on erythroid progenitors (CFU-E and BFU-E) in human CD34+ separated bone marrow cells and the relationship between insulin and erythropoietin. Stem Cells, 1994, 12(3), 329-338.
[http://dx.doi.org/10.1002/stem.5530120309] [PMID: 7521243]
[55]
Bersch, N.; Groopman, J.E.; Golde, D.W. Natural and biosynthetic insulin stimulates the growth of human erythroid progenitors in vitro. J. Clin. Endocrinol. Metab., 1982, 55(6), 1209-1211.
[http://dx.doi.org/10.1210/jcem-55-6-1209] [PMID: 6752170]
[56]
Ratajczak, J.; Zhang, Q.; Pertusini, E.; Wojczyk, B.S.; Wasik, M.A.; Ratajczak, M.Z. The role of insulin (INS) and insulin-like growth factor-I (IGF-I) in regulating human erythropoiesis. Studies in vitro under serum-free conditions--comparison to other cytokines and growth factors. Leukemia, 1998, 12(3), 371-381.
[http://dx.doi.org/10.1038/sj.leu.2400927] [PMID: 9529132]
[57]
Koenig, W.; Ernst, E. The possible role of hemorheology in atherothrombogenesis. Atherosclerosis, 1992, 94(2-3), 93-107.
[http://dx.doi.org/10.1016/0021-9150(92)90234-8] [PMID: 1632876]
[58]
Turitto, V.T.; Weiss, H.J. Platelet and red cell involvement in mural thrombogenesis. Ann. N. Y. Acad. Sci., 1983, 416, 363-376.
[http://dx.doi.org/10.1111/j.1749-6632.1983.tb35199.x] [PMID: 6587813]
[59]
LoPresti, R.; Montana, M.; Canino, B.; Ventimiglia, G.; Catania, A.; Caimi, G. Diabetes mellitus: Polymorphonuclear leukocyte (PMN) filtration parameters and PMN membrane fluidity after chemotactic activation. Metabolism, 1999, 48(1), 30-33.
[http://dx.doi.org/10.1016/S0026-0495(99)90006-9] [PMID: 9920141]