Associations of Insulin Resistance and High-Sensitivity C-Reactive Protein with Metabolic Abnormalities in Korean Patients with Type 2 Diabetes Mellitus: A Preliminary Study
Abstract
:1. Introduction
2. Patients and Methods
2.1. Study Patients and Setting
2.2. Data Collection
2.3. Assessment of IR
2.4. Patient Evaluation and Criteria
2.5. Statistical Analysis
3. Results
3.1. Baseline Characteristics of the Patients
3.2. Associations of IR and hsCRP with Metabolic Abnormalities
4. Discussion
- There was a significant positive association between the prevalence of SLD, MetS, albuminuria and diabetic retinopathy and KITT (p < 0.001).
- There was a significant positive association between the prevalence of SLD, MetS and albuminuria and hsCRP (p < 0.001).
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Rochlani, Y.; Pothineni, N.V.; Kovelamudi, S.; Mehta, J.L. Metabolic syndrome: Pathophysiology, management, and modulation by natural compounds. Ther. Adv. Cardiovasc. Dis. 2017, 11, 215–225. [Google Scholar] [CrossRef] [PubMed]
- Yun, J.S.; Jung, S.H.; Shivakumar, M.; Xiao, B.; Khera, A.V.; Won, H.H.; Kim, D. Polygenic risk for type 2 diabetes, lifestyle, metabolic health, and cardiovascular disease: A prospective UK Biobank study. Cardiovasc. Diabetol. 2022, 21, 131. [Google Scholar] [CrossRef] [PubMed]
- Jha, B.K.; Sherpa, M.L.; Imran, M.; Mohammed, Y.; Jha, L.A.; Paudel, K.R.; Jha, S.K. Progress in Understanding Metabolic Syndrome and Knowledge of Its Complex Pathophysiology. Diabetology 2023, 4, 134–159. [Google Scholar] [CrossRef]
- Zhao, X.; An, X.; Yang, C.; Sun, W.; Ji, H.; Lian, F. The crucial role and mechanism of insulin resistance in metabolic disease. Front. Endocrinol. 2023, 14, 1149239. [Google Scholar] [CrossRef] [PubMed]
- Mitrovic, B.; Gluvic, Z.M.; Obradovic, M.; Radunovic, M.; Rizzo, M.; Banach, M.; Isenovic, E.R. Non-alcoholic fatty liver disease, metabolic syndrome, and type 2 diabetes mellitus: Where do we stand today? Arch. Med. Sci. 2022, 19, 884–894. [Google Scholar] [CrossRef] [PubMed]
- Vetrano, E.; Rinaldi, L.; Mormone, A.; Giorgione, C.; Galiero, R.; Caturano, A.; Nevola, R.; Marfella, R.; Sasso, F.C. Non-alcoholic Fatty Liver Disease (NAFLD), Type 2 Diabetes, and Non-viral Hepatocarcinoma: Pathophysiological Mechanisms and New Therapeutic Strategies. Biomedicines 2023, 11, 468. [Google Scholar] [CrossRef] [PubMed]
- Wondmkun, Y.T. Obesity, Insulin Resistance, and Type 2 Diabetes: Associations and Therapeutic Implications. Diabetes Metab. Syndr. Obes. 2020, 13, 3611–3616. [Google Scholar] [CrossRef] [PubMed]
- Rohm, T.V.; Meier, D.T.; Olefsky, J.M.; Donath, M.Y. Inflammation in obesity, diabetes, and related disorders. Immunity 2022, 55, 31–55. [Google Scholar] [CrossRef] [PubMed]
- Chandrasekaran, P.; Weiskirchen, R. The Role of Obesity in Type 2 Diabetes Mellitus—An Overview. Int. J. Mol. Sci. 2024, 25, 1882. [Google Scholar] [CrossRef]
- Galicia-Garcia, U.; Benito-Vicente, A.; Jebari, S.; Larrea-Sebal, A.; Siddiqi, H.; Uribe, K.B.; Ostolaza, H.; Martín, C. Pathophysiology of Type 2 Diabetes Mellitus. Int. J. Mol. Sci. 2020, 21, 6275. [Google Scholar] [CrossRef]
- Cocea, A.-C.; Stoica, C.I. Interactions and Trends of Interleukins, PAI-1, CRP, and TNF-α in Inflammatory Responses during the Perioperative Period of Joint Arthroplasty: Implications for Pain Management—A Narrative Review. J. Pers. Med. 2024, 14, 537. [Google Scholar] [CrossRef] [PubMed]
- Speelman, T.; Dale, L.; Louw, A.; Verhoog, N.J.D. The Association of Acute Phase Proteins in Stress and Inflammation-Induced T2D. Cells 2022, 11, 2163. [Google Scholar] [CrossRef] [PubMed]
- Badoiu, S.C.; Enescu, D.M.; Tatar, R.; Stanescu-Spinu, I.-I.; Miricescu, D.; Greabu, M.; Ionel, I.P.; Jinga, V. Serum Plasminogen Activator Inhibitor-1, α 1-Acid Glycoprotein, C-Reactive Protein, and Platelet Factor 4 Levels—Promising Molecules That Can Complete the “Puzzle” of the Biochemical Milieu in Severe Burns: Preliminary Results of a Cohort Prospective Study. J. Clin. Med. 2024, 13, 2794. [Google Scholar] [CrossRef] [PubMed]
- Boncler, M.; Wu, Y.; Watala, C. The Multiple Faces of C-Reactive Protein—Physiological and Pathophysiological Implications in Cardiovascular Disease. Molecules 2019, 24, 2062. [Google Scholar] [CrossRef] [PubMed]
- Pickup, J.C.; Crook, M.A. Is Type II Diabetes Mellitus a Disease of the Innate Immune System? Diabetologia 1998, 41, 1241–1248. [Google Scholar] [CrossRef] [PubMed]
- Kolb, H.; Mandrup-Poulsen, T. An Immune Origin of Type 2 Diabetes? Diabetologia 2005, 48, 1038–1050. [Google Scholar] [CrossRef] [PubMed]
- Festa, A.; D’Agostino, R., Jr.; Howard, G.; Mykkanen, L.; Tracy, R.P.; Haffner, S.M. Chronic subclinical inflammation as part of the insulin resistance syndrome: The Insulin Resistance Atherosclerosis Study (IRAS). Circulation 2000, 102, 42–47. [Google Scholar] [CrossRef] [PubMed]
- Dandona, P.; Aljada, A.; Chaudhuri, A.; Mohanty, P.; Garg, R. Metabolic syndrome: A comprehensive perspective based on interactions between obesity, diabetes, and inflammation. Circulation 2005, 111, 1448–1454. [Google Scholar] [CrossRef] [PubMed]
- Kumar, R.; Nandhini, L.P.; Kamalanathan, S.; Sahoo, J.; Vivekanadan, M. Evidence for Current Diagnostic Criteria of Diabetes Mellitus. World J. Diabetes 2016, 7, 396–405. [Google Scholar] [CrossRef]
- Fonseca, V.A. Early Identification and Treatment of Insulin Resistance: Impact on Subsequent Prediabetes and Type 2 Diabetes. Clin. Cornerstone 2007, 8, S7–S18. [Google Scholar] [CrossRef]
- Baroncini, L.A.V.; de Castro Sylvestre, L.; Filho, R.P. Carotid Intima-Media Thickness and Carotid Plaque Represent Different Adaptive Responses to Traditional Cardiovascular Risk Factors. Int. J. Cardiol. Heart Vasc. 2015, 9, 48–51. [Google Scholar] [PubMed]
- Kälsch, A.I.; Csernok, E.; Münch, D.; Birck, R.; Yard, B.A.; Gross, W.; Kälsch, T.; Schmitt, W.H. Use of Highly Sensitive C-Reactive Protein for Followup of Wegener’s Granulomatosis. J. Rheumatol. 2010, 37, 2319–2325. [Google Scholar] [CrossRef]
- Hahn, M.K.; Giacca, A.; Pereira, S. In vivo techniques for assessment of insulin sensitivity and glucose metabolism. J. Endocrinol. 2024, 260, e230308. [Google Scholar] [CrossRef] [PubMed]
- Minh, H.V.; Tien, H.A.; Sinh, C.T.; Thang, D.C.; Chen, C.H.; Tay, J.C.; Siddique, S.; Wang, T.D.; Sogunuru, G.P.; Chia, Y.C.; et al. Assessment of preferred methods to measure insulin resistance in Asian patients with hypertension. J. Clin. Hypertens. 2021, 23, 529–537. [Google Scholar] [CrossRef]
- Okita, K.; Iwahashi, H.; Kozawa, J.; Okauchi, Y.; Funahashi, T.; Imagawa, A.; Shimomura, I. Usefulness of the Insulin Tolerance Test in Patients with Type 2 Diabetes Receiving Insulin Therapy. J. Diabetes Investig. 2014, 5, 305–312. [Google Scholar] [CrossRef] [PubMed]
- Bonora, E.; Moghetti, P.; Zancanaro, C.; Cigolini, M.; Querena, M.; Cacciatori, V.; Corgnati, A.; Muggeo, M. Estimates of in vivo insulin action in man: Comparison of insulin tolerance tests with euglycemic and hyperglycemic glucose clamp studies. J. Clin. Endocrinol. Metab. 1989, 68, 374–378. [Google Scholar] [CrossRef] [PubMed]
- Park, S.W.; Yun, Y.S.; Ahn, C.W.; Nam, J.H.; Kwon, S.H.; Song, M.K.; Han, S.H.; Cha, B.S.; Son, Y.D.; Lee, H.C.; et al. Short Insulin Tolerance Test (SITT) for the Determination of In Vivo Insulin Sensitivity-A Comparison with Euglycemic Clamp Test. J. Korean Diabetes Assoc. 1998, 22, 199–208. [Google Scholar]
- Engwerda, E.E.; Abbink, E.J.; Tack, C.J.; de Galan, B.E. Improved Pharmacokinetic and Pharmacodynamic Profile of Rapid-Acting Insulin Using Needle-Free Jet Injection Technology. Diabetes Care 2011, 34, 1804–1808. [Google Scholar] [CrossRef] [PubMed]
- Drabsch, T.; Holzapfel, C.; Stecher, L.; Petzold, J.; Skurk, T.; Hauner, H. Associations Between C-Reactive Protein, Insulin Sensitivity, and Resting Metabolic Rate in Adults: A Mediator Analysis. Front. Endocrinol. 2018, 9, 556. [Google Scholar] [CrossRef]
- Chen, L.; Chen, R.; Wang, H.; Liang, F. Mechanisms Linking Inflammation to Insulin Resistance. Int. J. Endocrinol. 2015, 2015, 508409. [Google Scholar] [CrossRef]
- Xu, W.; Tian, M.; Zhou, Y. The relationship between insulin resistance, adiponectin and C-reactive protein and vascular endothelial injury in diabetic patients with coronary heart disease. Exp. Ther. Med. 2018, 16, 2022–2026. [Google Scholar] [CrossRef] [PubMed]
- Yousuf, O.; Mohanty, B.D.; Martin, S.S.; Joshi, P.H.; Blaha, M.J.; Nasir, K.; Blumenthal, R.S.; Budoff, M.J. High-sensitivity C-reactive protein and cardiovascular disease: A resolute belief or an elusive link? J. Am. Coll. Cardiol. 2013, 62, 397–408. [Google Scholar] [CrossRef] [PubMed]
- Pérez-Martin, A.; Raynaud, E.; Mercier, J. Insulin Resistance and Associated Metabolic Abnormalities in Muscle: Effects of Exercise. Obes. Rev. 2001, 2, 47–59. [Google Scholar] [CrossRef] [PubMed]
- Roberts, C.K.; Hevener, A.L.; Barnard, R.J. Metabolic Syndrome and Insulin Resistance: Underlying Causes and Modification by Exercise Training. Compr. Physiol. 2013, 3, 1–58. [Google Scholar] [PubMed]
- Meigs, J.B.; Rutter, M.K.; Sullivan, L.M.; Fox, C.S.; D’Agostino, R.B., Sr.; Wilson, P.W. Impact of Insulin Resistance on Risk of Type 2 Diabetes and Cardiovascular Disease in People with Metabolic Syndrome. Diabetes Care 2007, 30, 1219–1225. [Google Scholar] [CrossRef] [PubMed]
- Vesa, C.M.; Popa, L.; Popa, A.R.; Rus, M.; Zaha, A.A.; Bungau, S.; Tit, D.M.; Corb Aron, R.A.; Zaha, D.C. Current Data Regarding the Relationship between Type 2 Diabetes Mellitus and Cardiovascular Risk Factors. Diagnostics 2020, 10, 314. [Google Scholar] [CrossRef] [PubMed]
- Magkos, F.; Yannakoulia, M.; Chan, J.L.; Mantzoros, C.S. Management of the Metabolic Syndrome and Type 2 Diabetes through Lifestyle Modification. Annu. Rev. Nutr. 2009, 29, 223–256. [Google Scholar] [CrossRef] [PubMed]
- Del Prato, S.; Penno, G.; Miccoli, R. Changing the Treatment Paradigm for Type 2 Diabetes. Diabetes Care 2009, 32, S217–S222. [Google Scholar] [CrossRef] [PubMed]
- Vesković, M.; Šutulović, N.; Hrnčić, D.; Stanojlović, O.; Macut, D.; Mladenović, D. The Interconnection between Hepatic Insulin Resistance and Metabolic Dysfunction-Associated Steatotic Liver Disease—The Transition from an Adipocentric to Liver-Centric Approach. Curr. Issues Mol. Biol. 2023, 45, 9084–9102. [Google Scholar] [CrossRef]
- Hutchison, A.L.; Tavaglione, F.; Romeo, S.; Charlton, M. Endocrine aspects of metabolic dysfunction associated steatotic liver disease (MASLD): Beyond insulin resistance. J. Hepatol. 2023, 79, 1524–1541. [Google Scholar] [CrossRef]
- Leite, N.C.; Villela-Nogueira, C.A.; Cardoso, C.R.; Salles, G.F. Non-Alcoholic Fatty Liver Disease and Diabetes: From Physiopathological Interplay to Diagnosis and Treatment. World J. Gastroenterol. 2014, 20, 8377–8392. [Google Scholar] [CrossRef] [PubMed]
- Zeng, P.; Cai, X.; Yu, X.; Gong, L. Markers of insulin resistance associated with non-alcoholic fatty liver disease in non-diabetic population. Sci. Rep. 2023, 13, 20470. [Google Scholar] [CrossRef] [PubMed]
- Solomon, A.; Negrea, M.O.; Cipăian, C.R.; Boicean, A.; Mihaila, R.; Rezi, C.; Cristinescu, B.A.; Berghea-Neamtu, C.S.; Popa, M.L.; Teodoru, M.; et al. Interactions between Metabolic Syndrome, MASLD, and Arterial Stiffening: A Single-Center Cross-Sectional Study. Healthcare 2023, 11, 2696. [Google Scholar] [CrossRef]
- Zhang, J.; Zhao, Y.; Xu, C.; Hong, Y.; Lu, H.; Wu, J.; Chen, Y. Association between Serum Free Fatty Acid Levels and Nonalcoholic Fatty Liver Disease: A Cross-Sectional Study. Sci. Rep. 2014, 4, 5832. [Google Scholar] [CrossRef]
- Bril, F.; Cusi, K. Management of Nonalcoholic Fatty Liver Disease in Patients with Type 2 Diabetes: A Call to Action. Diabetes Care 2017, 40, 419–430. [Google Scholar] [CrossRef]
- Stehouwer, C.D.; Smulders, Y.M. Microalbuminuria and Risk for Cardiovascular Disease: Analysis of Potential Mechanisms. J. Am. Soc. Nephrol. 2006, 17, 2106–2111. [Google Scholar] [CrossRef]
- Bornfeldt, K.E.; Tabas, I. Insulin Resistance, Hyperglycemia, and Atherosclerosis. Cell Metab. 2011, 14, 575–585. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.A.; Montagnani, M.; Koh, K.K.; Quon, M.J. Reciprocal Relationships between Insulin Resistance and Endothelial Dysfunction: Molecular and Pathophysiological Mechanisms. Circulation 2006, 113, 1888–1904. [Google Scholar] [CrossRef] [PubMed]
- El-Atat, F.A.; Stas, S.N.; McFarlane, S.I.; Sowers, J.R. The Relationship between Hyperinsulinemia, Hypertension and Progressive Renal Disease. J. Am. Soc. Nephrol. 2004, 15, 2816–2827. [Google Scholar] [CrossRef]
- Welsh, G.I.; Coward, R.J. Podocytes, Glucose and Insulin. Curr. Opin. Nephrol. Hypertens. 2010, 19, 379–384. [Google Scholar] [CrossRef]
- De Cosmo, S.; Menzaghi, C.; Prudente, S.; Trischitta, V. Role of Insulin Resistance in Kidney Dysfunction: Insights into the Mechanism and Epidemiological Evidence. Nephrol. Dial. Transplant. 2013, 28, 29–36. [Google Scholar] [CrossRef] [PubMed]
- Jauregui, A.; Mintz, D.H.; Mundel, P.; Fornoni, A. Role of Altered Insulin Signaling Pathways in the Pathogenesis of Podocyte Malfunction and Microalbuminuria. Curr. Opin. Nephrol. Hypertens. 2009, 18, 539–545. [Google Scholar] [CrossRef] [PubMed]
- Haffner, S.M.; D’Agostino, R., Jr.; Mykkänen, L.; Tracy, R.; Howard, B.; Rewers, M.; Selby, J.; Savage, P.J.; Saad, M.F. Insulin Sensitivity in Subjects with Type 2 Diabetes. Relationship to Cardiovascular Risk Factors: The Insulin Resistance Atherosclerosis Study. Diabetes Care 1999, 22, 562–568. [Google Scholar] [CrossRef] [PubMed]
- Kuusisto, J.; Lempiäinen, P.; Mykkänen, L.; Laakso, M. Insulin Resistance Syndrome Predicts Coronary Heart Disease Events in Elderly Type 2 Diabetic Men. Diabetes Care 2001, 24, 1629–1633. [Google Scholar] [CrossRef] [PubMed]
- Klein, R.; Klein, B.E.; Moss, S.E. Epidemiology of Proliferative Diabetic Retinopathy. Diabetes Care 1992, 15, 1875–1891. [Google Scholar] [CrossRef] [PubMed]
- Hamirani, Y.S.; Katz, R.; Nasir, K.; Zeb, I.; Blaha, M.J.; Blumenthal, R.S.; Kronmal, R.N.; Budoff, M.J. Association between inflammatory markers and liver fat: The Multi-Ethnic Study of Atherosclerosis. J. Clin. Exp. Cardiol. 2014, 5, 1000344. [Google Scholar] [CrossRef] [PubMed]
- Ridker, P.M.; Buring, J.E.; Cook, N.R.; Rifai, N. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: An 8-year follow-up of 14,719 initially healthy American women. Circulation 2003, 107, 391–397. [Google Scholar] [CrossRef] [PubMed]
- Duncan, B.B.; Schmidt, M.I.; Pankow, J.S.; Ballantyne, C.M. Low-grade systemic inflammation and the development of type 2 diabetes: The Atherosclerosis Risk in Communities study. Diabetes 2003, 52, 1799–1805. [Google Scholar] [CrossRef] [PubMed]
- Fröhlich, M.; Imhof, A.; Berg, G.; Hutchinson, W.L.; Pepys, M.B.; Boeing, H.E.I.N.; Muche, R.; Brenner, H.; Koenig, W. Association between C-reactive protein and features of the metabolic syndrome: A population-based study. Diabetes Care 2000, 23, 1835–1839. [Google Scholar] [CrossRef]
- Promrat, K.; Lutchman, G.; Uwaifo, G.I.; Freedman, R.J.; Soza, A.; Heller, T.; Doo, E.; Ghany, M.; Premkumar, A.; Park, Y.; et al. A pilot study of pioglitazone treatment for nonalcoholic steatohepatitis. Hepatology 2004, 39, 188–196. [Google Scholar] [CrossRef]
- Nervi, F.; Miquel, J.F.; Alvarez, M.; Ferreccio, C.; García-Zattera, M.J.; González, R.; Pérez-Ayuso, R.M.; Rigotti, A.; Villarroel, L. Gallbladder disease is associated with insulin resistance in a high-risk Hispanic population. J. Hepatol. 2006, 45, 299–305. [Google Scholar] [CrossRef]
- Marchesini, G.; Brizi, M.; Bianchi, G.; Tomassetti, S.; Bugianesi, E.; Lenzi, M.; McCullough, A.J.; Natale, S.; Forlani, G. Nonalcoholic fatty liver disease: A feature of the metabolic syndrome. Diabetes 2001, 50, 1844–1850. [Google Scholar] [CrossRef] [PubMed]
- Angelico, F.; Del Ben, M.; Conti, R.; Francioso, S.; Feole, K.; Maccioni, D.; Antonini, T.M.; Alessandri, C. Non-alcoholic fatty liver syndrome: A hepatic consequence of common metabolic diseases. J. Gastroenterol. Hepatol. 2003, 18, 588–594. [Google Scholar] [CrossRef] [PubMed]
- Tsioufis, C.; Dimitriadis, K.; Taxiarchou, E.; Vasiliadou, C.; Chartzoulakis, G.; Tousoulis, D.; Manolis, A.; Stefanadis, C.; Kallikazaros, I. Diverse associations of microalbuminuria with C-reactive protein, interleukin-18, and soluble CD 40 ligand in male essential hypertensive subjects. Am. J. Hypertens. 2006, 19, 462–466. [Google Scholar] [CrossRef]
- Pedrinelli, R.; Dell’Omo, G.; Di Bello, V.; Pellegrini, G.; Pucci, L.; Del Prato, S.; Penno, G. Low-grade inflammation and microalbuminuria in hypertension. Arterioscler. Thromb. Vasc. Biol. 2004, 24, 2414–2419. [Google Scholar] [CrossRef] [PubMed]
- Tsioufis, C.; Dimitriadis, K.; Antoniadis, D.; Stefanadis, C.; Kallikazaros, I. Inter-relationships of microalbuminuria with the other surrogates of the atherosclerotic cardiovascular disease in hypertensive subjects. Am. J. Hypertens. 2004, 17, 470–476. [Google Scholar] [CrossRef] [PubMed]
- Pannacciulli, N.; Cantatore, F.P.; Minenna, A.; Bellacicco, M.; Giorgino, R.; De Pergola, G. Urinary albumin excretion is independently associated with C-reactive protein levels in overweight and obese nondiabetic premenopausal women. J. Intern. Med. 2001, 250, 502–527. [Google Scholar] [CrossRef]
- Jager, A.; van Hinsbergh, V.W.; Kostense, P.J.; Emeis, J.J.; Nijpels, G.; Dekker, J.M.; Heine, R.J.; Bouter, L.M.; Stehouwer, C.D. C-reactive protein and soluble vascular cell adhesion molecule-1 are associated with elevated urinary albumin excretion but do not explain its link with cardiovascular risk. Arterioscler. Thromb. Vasc. Biol. 2002, 22, 593–598. [Google Scholar] [CrossRef]
- Barzilay, J.I.; Peterson, D.; Cushman, M.; Heckbert, S.R.; Cao, J.J.; Blaum, C.; Tracy, R.P.; Klein, R.; Herrington, D.M. The relationship of cardiovascular risk factors to microalbuminuria in older adults with or without diabetes mellitus or hypertension: The Cardiovascular Health Study. Am. J. Kidney Dis. 2004, 44, 25–34. [Google Scholar] [CrossRef]
- Tang, P.M.; Zhang, Y.Y.; Hung, J.S.; Chung, J.Y.; Huang, X.R.; To, K.F.; Lan, H.Y. DPP4/CD32b/NF-κB Circuit: A Novel Druggable Target for Inhibiting CRP-Driven Diabetic Nephropathy. Mol. Ther. 2021, 29, 365–375. [Google Scholar] [CrossRef]
- Hart, P.C.; Rajab, I.M.; Alebraheem, M.; Potempa, L.A. C-Reactive Protein and Cancer-Diagnostic and Therapeutic Insights. Front. Immunol. 2020, 11, 595835. [Google Scholar] [CrossRef] [PubMed]
- Libby, P. Inflammation in Atherosclerosis-No Longer a Theory. Clin. Chem. 2021, 67, 131–142. [Google Scholar] [CrossRef] [PubMed]
- Aktas, G.; Atak Tel, B.M.; Tel, R.; Balci, B. Treatment of type 2 diabetes patients with heart conditions. Expert. Rev. Endocrinol. Metab. 2023, 18, 255–265. [Google Scholar] [CrossRef] [PubMed]
- Wellen, K.E.; Hotamisligil, G.S. Obesity-induced inflammatory changes in adipose tissue. J. Clin. Investig. 2003, 112, 1785–1788. [Google Scholar] [CrossRef] [PubMed]
- Lim, S.; Lee, H.K.; Kimm, K.C.; Park, C.; Shin, C.; Cho, N.H. C-reactive protein level as an independent risk factor of metabolic syndrome in the Korean population: CRP as risk factor of metabolic syndrome. Diabetes Res. Clin. Pract. 2005, 70, 126–133. [Google Scholar] [CrossRef] [PubMed]
- Ryu, S.Y.; Kim, K.S.; Park, J.; Kang, M.G.; Han, M.A. The association between circulating inflammatory markers and metabolic syndrome in Korean rural adults. J. Prev. Med. Public Health 2008, 41, 413–418. [Google Scholar] [CrossRef]
- Ye, X.; Yu, Z.; Li, H.; Franco, O.H.; Liu, Y.; Lin, X. Distributions of C-reactive protein and its association with metabolic syndrome in middle-aged and older Chinese people. J. Am. Coll. Cardiol. 2007, 49, 1798–1805. [Google Scholar] [CrossRef]
- Cheal, K.L.; Abbasi, F.; Lamendola, C.; McLaughlin, T.; Reaven, G.M.; Ford, E.S. Relationship to insulin resistance of the adult treatment panel III diagnostic criteria for identification of the metabolic syndrome. Diabetes 2004, 53, 1195–1200. [Google Scholar] [CrossRef] [PubMed]
- Carr, D.B.; Utzschneider, K.M.; Hull, R.L.; Kodama, K.; Retzlaff, B.M.; Brunzell, J.D.; Shofer, J.B.; Fish, B.E.; Knopp, R.H.; Kahn, S.E. Intra-abdominal fat is a major determinant of the National Cholesterol Education Program Adult Treatment Panel III criteria for the metabolic syndrome. Diabetes 2004, 53, 2087–2094. [Google Scholar] [CrossRef]
- den Engelsen, C.; Koekkoek, P.S.; Gorter, K.J.; van den Donk, M.; Salomé, P.L.; Rutten, G.E. High-sensitivity C-reactive protein to detect metabolic syndrome in a centrally obese population: A cross-sectional analysis. Cardiovasc. Diabetol. 2012, 11, 25. [Google Scholar] [CrossRef]
- Boden, G.; Shulman, G.I. Free fatty acids in obesity and type 2 diabetes: Defining their role in the development of insulin resistance and beta-cell dysfunction. Eur. J. Clin. Investig. 2002, 32 (Suppl. S3), 14–23. [Google Scholar] [CrossRef] [PubMed]
- Fahed, G.; Aoun, L.; Bou Zerdan, M.; Allam, S.; Bou Zerdan, M.; Bouferraa, Y.; Assi, H.I. Metabolic Syndrome: Updates on Pathophysiology and Management in 2021. Int. J. Mol. Sci. 2022, 23, 786. [Google Scholar] [CrossRef] [PubMed]
- Zhao, J.; Wu, Y.; Rong, X.; Zheng, C.; Guo, J. Anti-Lipolysis Induced by Insulin in Diverse Pathophysiologic Conditions of Adipose Tissue. Diabetes Metab. Syndr. Obes. 2020, 13, 1575–1585. [Google Scholar] [CrossRef] [PubMed]
- Paredes, S.; Fonseca, L.; Ribeiro, L.; Ramos, H.; Oliveira, J.C.; Palma, I. Novel and traditional lipid profiles in Metabolic Syndrome reveal a high atherogenicity. Sci. Rep. 2019, 9, 11792. [Google Scholar] [CrossRef] [PubMed]
- Souza, J.R.; Oliveira, R.T.; Blotta, M.H.; Coelho, O.R. Serum levels of interleukin-6 (Il-6), interleukin-18 (Il-18) and C-reactive protein (CRP) in patients with type-2 diabetes and acute coronary syndrome without ST-segment elevation. Arq. Bras. Cardiol. 2008, 90, 86–90. [Google Scholar]
- Geer, E.B.; Shen, W. Gender differences in insulin resistance, body composition, and energy balance. Gend. Med. 2009, 6, 60–75. [Google Scholar] [CrossRef]
Variables | Values | p for Trend | ||
---|---|---|---|---|
Tertile 1 (n = 1255) | Tertile 2 (n = 1267) | Tertile 3 (n = 1236) | ||
KITT | 3.18 ± 0.67 | 1.93 ± 0.23 a | 1.08 ± 0.31 a,b | <0.001 |
Age (years old) | 56.47 ± 9.95 | 57.86 ± 10.12 a | 58.46 ± 10.71 a | <0.001 |
Duration (years) | 6.94 ± 6.85 | 7.63 ± 7.23 a | 8.68 ± 7.30 a,b | <0.001 |
Sex (men, %) | 669 (53.3%) | 637 (50.3%) | 646 (52.3%) | |
SBP (mmHg) | 132.08 ± 16.63 | 136.97 ± 17.95 a | 138.02 ± 18.94 a | <0.001 |
DBP (mmHg) | 84.18 ± 11.06 | 86.24 ± 11.48 a | 87.09 ± 11.82 a | <0.001 |
Waist (cm) | 81.42 ± 8.15 | 83.99 ± 8.18 a | 86.31 ± 8.56 a,b | <0.001 |
BMI (kg/m2) | 23.90 ± 2.89 | 24.69 ± 2.96 a | 25.36 ± 3.43 a,b | <0.001 |
VFT (mm) | 39.95 ± 16.47 | 45.61 ± 17.30 a | 50.20 ± 18.78 a,b | <0.001 |
Fasting plasma insulin (nmol/IU) | 7.38 ± 3.91 | 8.53 ± 4.30 a | 10.20 ± 5.47 a,b | <0.001 |
C-peptide (nmol/L) | 1.69 ± 0.72 | 1.96 ± 0.79 a | 2.31 ± 1.02 a,b | <0.001 |
HbA1c (%) | 7.65 ± 1.61 | 8.20 ± 1.82 a | 8.99 ± 2.06 a,b | <0.001 |
FPG (mg/dL) | 138.31 ± 41.06 | 154.25 ± 52.30 a | 185.20 ± 67.18 a,b | <0.001 |
PPG (mg/dL) | 201.62 ± 80.96 | 227.40 ± 84.30 a | 271.57 ± 91.29 a,b | <0.001 |
HOMA-IR | 2.49 ± 1.45 | 3.17 ± 1.80 a | 4.53 ± 2.84 a,b | <0.001 |
HOMA-β | 49.85 ± 66.66 | 48.76 ± 52.30 | 43.08 ± 47.96 a,b | <0.006 |
AST (U/L) | 25.00 ± 10.21 | 26.39 ± 12.30 a | 30.30 ± 16.38 a,b | <0.001 |
ALT (U/L) | 25.81 ± 16.93 | 29.10 ± 19.38 a | 34.49 ± 25.39 a,b | <0.001 |
Total cholesterol (mg/dL) | 189.82 ± 38.41 | 198.33 ± 38.24 a | 201.59 ± 43.96 a | <0.001 |
TG (mg/dL) | 121.74 ± 73.54 | 150.22 ± 97.37 a | 183.62 ± 136.10 a,b | <0.001 |
HDL-C (mg/dL) | 51.38 ± 13.47 | 50.09 ± 13.12 a | 48.24 ± 12.75 a,b | <0.001 |
LDL-C (mg/dL) | 112.13 ± 32.64 | 116.95 ± 33.02 | 117.47 ± 36.41 a | <0.001 |
Albuminuria (g/L) | 37.57 ± 51.90 | 48.42 ± 56.68 a | 69.30 ± 68.60 a,b | <0.001 |
IMT | 0.82 ± 0.17 | 0.84 ± 0.18 a | 0.85 ± 0.18 a | <0.001 |
Max IMT (mm) | 0.89 ± 0.20 | 0.91 ± 0.21 a | 0.92 ± 0.21 a | <0.001 |
CRP (mg/L) | 1.47 ± 3.48 | 1.78 ± 4.72 | 2.72 ± 7.61 a,b | <0.001 |
Variables | Values | p for Trend | |||
---|---|---|---|---|---|
Tertile 1 (n = 1255) | Tertile 2 (n = 1267) | Tertile 3 (n = 1236) | |||
KITT | |||||
Steatotic liver disease | 448 (24.40%) | 645 (35.10%) | 743 (66.20%) | <0.001 | |
Metabolic syndrome | 424 (11.50%) | 606 (16.50%) | 739 (20.10%) | <0.001 | |
Albuminuria | 342 (30.40%) | 505 (43.80%) | 653 (57.50%) | <0.001 | |
Diabetic retinopathy | 65 (5.30%) | 102 (8.20%) | 126 (10.50%) | <0.001 | |
hsCRP | |||||
Steatotic liver disease | 446 (41.80%) | 647 (58.50%) | 743 (65.20%) | <0.001 | |
Metabolic syndrome | 411 (34.10%) | 626 (50.80%) | 732 (59.00%) | <0.001 | |
Albuminuria | 401 (36.50%) | 510 (44.90%) | 589 (50.00%) | <0.001 | |
Diabetic retinopathy | 115 (9.40%) | 93 (7.70%) | 85 (6.90%) | <0.020 |
Variables | Values | |||||
---|---|---|---|---|---|---|
Tertile 1 (n = 1255) | Tertile 2 (n = 1267) | Tertile 3 (n = 1236) | ||||
OR (95% CI) | OR (95% CI) | p | OR (95% CI) | p | ||
KITT | ||||||
Steatotic liver disease | 1.00 | 1.756 (1.409–2.189) | <0.001 | 2.499 (1.968–3.714) | <0.001 | |
Metabolic syndrome | 1.00 | 1.836 (1.561–2.159) | <0.001 | 2.971 (2.520–3.503) | <0.001 | |
Albuminuria | 1.00 | 1.782 (1.500–2.117) | <0.001 | 3.098 (2.605–3.684) | <0.001 | |
Diabetic retinopathy | 1.00 | 1.580 (1.146–2.180) | <0.005 | 2.066 (1.514–2.819) | <0.001 | |
hsCRP | ||||||
Steatotic liver disease | 1.00 | 1.960 (1.652–2.324) | <0.001 | 2.602 (2.190–3.091) | <0.001 | |
Metabolic syndrome | 1.00 | 1.995 (1.694–2.349) | <0.001 | 2.782 (2.360–3.278) | <0.001 | |
Albuminuria | 1.00 | 1.416 (1.195–1.678) | <0.001 | 1.738 (1.470–2.056) | <0.001 | |
Diabetic retinopathy | 1.00 | 0.795 (0.597–1.058) | <0.116 | 0.710 (0.530–0.950) | <0.021 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Jeong, Y.; Lee, B.J.; Hur, W.; Lee, M.; Han, S.-H. Associations of Insulin Resistance and High-Sensitivity C-Reactive Protein with Metabolic Abnormalities in Korean Patients with Type 2 Diabetes Mellitus: A Preliminary Study. Metabolites 2024, 14, 371. https://doi.org/10.3390/metabo14070371
Jeong Y, Lee BJ, Hur W, Lee M, Han S-H. Associations of Insulin Resistance and High-Sensitivity C-Reactive Protein with Metabolic Abnormalities in Korean Patients with Type 2 Diabetes Mellitus: A Preliminary Study. Metabolites. 2024; 14(7):371. https://doi.org/10.3390/metabo14070371
Chicago/Turabian StyleJeong, Yuchul, Beom Jun Lee, Wonjai Hur, Minjoon Lee, and Se-Hyeon Han. 2024. "Associations of Insulin Resistance and High-Sensitivity C-Reactive Protein with Metabolic Abnormalities in Korean Patients with Type 2 Diabetes Mellitus: A Preliminary Study" Metabolites 14, no. 7: 371. https://doi.org/10.3390/metabo14070371