Powiadomienia systemowe
- Sesja wygasła!
Tytuł artykułu
Autorzy
Identyfikatory
Warianty tytułu
Języki publikacji
Abstrakty
Insulin resistance (IR) is a multifactorial metabolic disorder associated with the development of cardiometabolic syndrome, cardiovascular diseases and obesity. Factors such as inflammation, hyperinsulinemia, hyperglucagonemia, mitochondrial dysfunction, glucotoxicity and lipotoxicity contribute to the development of IR. Despite being extensively studied for over 60 years, assessing the incidence of IR, developing effective prevention strategies, and implementing appropriate therapeutic approaches remain challenging. This review explores the multifaceted nature of IR, including its association with various conditions such as obesity, primary hypertension, dyslipidemia, obstructive sleep apnea, Alzheimer’s disease, non-alcoholic fatty liver disease, polycystic ovary syndrome, chronic kidney disease and cancer. Additionally, we discuss the complexity of diagnosing and quantifying IR, emphasizing the lack of absolute, common criteria for classification. We delve into the use of mathematical models in clinical and epidemiological studies, focusing on the choice between insulin, triglycerides, or waist-to-hip ratio as IR determinants. Furthermore, we highlight the importance of reliable input data and caution in interpreting results when utilizing mathematical models for IR assessment. This narrative review aims to provide insights into the challenges and considerations involved in conducting IR diagnostics, with implications for clinical practice, epidemiological research, and future advancements in this field.
Wydawca
Czasopismo
Rocznik
Tom
Strony
55--67
Opis fizyczny
Bibliogr. 161 poz., rys., tab.
Twórcy
autor
- Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, Warsaw, Poland
autor
- Nalecz Institute of Biocybernetics and Biomedical Engineering, Polish Academy of Sciences, 4 Trojdena Street, 02-109 Warsaw, Poland
Bibliografia
- [1] Vague P. Résistance à l’insuline. Une place en santé ublique [Insulin resistance. A public health problem]. Ann Endocrinol (Paris) 1999;60(3):177-178. French.
- [2] Krentz AJ. Fortnightly Review: Insulin resistance. BMJ 1996;313:1385-9. https://doi.org/10.1136/bmj.313.7069.1385.
- [3] Kahn BB, Flier JS. Obesity and insulin resistance. J Clin Invest 2000;106(4): 473-81.
- [4] Lee SH, Park SY, Choi CS. Insulin resistance: from mechanisms to therapeutic strategies. Diabetes Metab J 2022;46(1):15-37. https://doi.org/10.4093/dmj.2021.0280.
- [5] Bergman RN, Piccinini F, Kabir M, Kolka CM, Ader M. Hypothesis: role of reduced hepatic insulin clearance in the pathogenesis of type 2 diabetes. Diabetes 2019;68 (9):1709-16. https://doi.org/10.2337/db19-0098.
- [6] Takano C, Ogawa E, Hayakawa S. Insulin resistance in mitochondrial diabetes. Biomolecules 2023;13(1):126.
- [7] Perumalsamy S, Huri HZ, Abdullah BM, Mazlan O, Wan Ahmad WA, Vethakkan SRDB. Genetic markers of insulin resistance and atherosclerosis in type 2 diabetes mellitus patients with coronary artery disease. Metabolites 2023; 13(3):427. https://doi.org/10.3390/metabo13030427.
- [8] Kahn R, Buse J, Ferrannini E, Stern M. The metabolic syndrome: time for a critical appraisal Joint Statement from the American Diabetes Association and the European Association for the Study of Diabetes. Diabetes Care 2005;28(9): 2289-304. https://doi.org/10.2337/diacare.28.9.2289.
- [9] Hill MA, Yang Y, Zhang L, Sun Z, Jia G, Parrish AR, et al. Insulin resistance, cardiovascular stiffening and cardiovascular disease. Metabolism 2021;119: 154766. https://doi.org/10.1016/j.metabol.2021.154766.
- [10] Kosmas CE, Bousvarou MD, Kostara CE, Papakonstantinou EJ, Salamou E, Guzman E. Insulin resistance and cardiovascular disease. J Int Med Res 2023;51 (3). https://doi.org/10.1177/03000605231164548.
- [11] Wang T, Li M, Zeng T, Hu R, Xu Y, Xu M, et al. Association between insulin resistance and cardiovascular disease risk varies according to glucose tolerance status: a nationwide prospective cohort study. Diabetes Care 2022;45(8): 1863-72. https://doi.org/10.2337/dc22-0202.
- [12] Correale M, Paolillo S, Mercurio V, Ruocco G, Tocchetti CG, Palazzuoli A. Noncardiovascular comorbidities in heart failure patients and their impact on prognosis. Kardiol Pol 2021;79(5):493-502. https://doi.org/10.33963/KP.15934.
- [13] Zhou X, Kang C, Hu Y, Wang X. Study on insulin resistance and ischemic cerebrovascular disease: A bibliometric analysis via CiteSpace. Front Public Health 2023;11:1021378. https://doi.org/10.3389/fpubh.2023.1021378.
- [14] Màrmol JM, Carlsson M, Raun SH, Grand MK, Sørensen J, Lang Lehrskov L, et al. Insulin resistance in patients with cancer: a systematic review and meta-analysis. Acta Oncol 2023;62(4):364-71. https://doi.org/10.1080/ 0284186X.2023.2197124.
- [15] Gallagher EJ, LeRoith D. Hyperinsulinaemia in cancer. Nat Rev Cancer 2020;20 (11):629-44. https://doi.org/10.1038/s41568-020-0295-5.
- [16] Zhang AMY, Xia YH, Lin JSH, Chu KH, Wang WCK, Ruiter TJJ, et al. Hyperinsulinemia acts via acinar insulin receptors to initiate pancreatic cancer by increasing digestive enzyme production and inflammation. Cell Metab 2023;35 (12):2093-250. https://doi.org/10.1016/j.cmet.2023.10.003.
- [17] Good to Know: All About Insulin Resistance. Clin Diabetes 2018;36(3):263-264.
- [18] Kahn SE, Hull RLM, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 2006; 444:(7121)840-846. https://doi.org/10.1038/nature05482.
- [19] Rohm TV, Meier DT, Olefsky JM, Donath MY. Inflammation in obesity, diabetes, and related disorders. Immunity 2022;55(1):31-55. https://doi.org/10.1016/j.immuni.2021.12.013.
- [20] Stefan N. Causes, consequences, and treatment of metabolically unhealthy fat distribution. Lancet Diabetes Endocrinol 2020;8(7):616-27. https://doi.org/10.1016/S2213-8587(20)30110-8.
- [21] Stefan N, Schulze MB. Metabolic health and cardiometabolic risk clusters: implications for prediction, prevention, and treatment. Lancet Diabetes Endocrinol 2023;11(6):426-40. https://doi.org/10.1016/S2213-8587(23)00086-4.
- [22] Colosimo S, Mitra SK, Chaudhury T, Marchesini G. Insulin resistance and metabolic flexibility as drivers of liver and cardiac disease in T2DM. Diabetes Res Clin Pract 2023;206:111016. https://doi.org/10.1016/j.diabres.2023.111016.
- [23] Patel P, Abate N. Body fat distribution and insulin resistance. Nutrients 2013;5: 2019-27. https://doi.org/10.3390/nu5062019.
- [24] Nolan CJ, Ruderman NB, Prentki M. Intensive insulin for type 2 diabetes: the risk of causing harm. Lancet Diabetes Endocrinol 2013;1(1):9-10. https://doi.org/10.1016/S2213-8587(13)70027-5.
- [25] Nolan CJ, Ruderman NB, Kahn SE, Pedersen O, Prentki M. Insulin resistance as a physiological defense against metabolic stress: implications for the management of subsets of type 2 diabetes. Diabetes 2015;64(3):673-86. https://doi.org/ 10.2337/db14-0694.
- [26] Reaven G, Abbasi F, McLaughlin T. Obesity. insulin resistance. and cardiovascular disease. Recent Prog Horm Res 2004;59:207-23. https://doi.org/10.1210/rp.59.1.207.
- [27] Ferrannini E, Natali A, Bell P, Cavallo-Perin P, Lalic N, Mingrone G. Insulin resistance and hypersecretion in obesity. European Group for the Study of Insulin Resistance (EGIR). J Clin Invest 1997;100(5):1166-73. https://doi.org/10.1172/ JCI119628.
- [28] Kelley DE, Goodpaster BH. Effects of physical activity on insulin action and glucose tolerance in obesity. Med Sci Sports Exerc 1999 (11 Suppl):S619-623. https://doi.org/10.1097/00005768-199911001-00021.
- [29] Chow LS, Gerszten RE, Taylor JM, Pedersen BK, van Praag H, Trappe S, et al. Exerkines in health, resilience and disease. Nat Rev Endocrinol 2022;18(5): 273-89. https://doi.org/10.1038/s41574-022-00641-2.
- [30] Balkau B, Mhamdi L, Oppert JM, Nolan J, Golay A, Porcellati F, et al. EGIR-RISC Study Group. Physical activity and insulin sensitivity: the RISC study. Diabetes 2008;57(10):2613-8. https://doi.org/10.2337/db07-1605.
- [31] Assah FK, Brage S, Ekelund U, Wareham NJ. The association of intensity and overall level of physical activity energy expenditure with a marker of insulin resistance. Diabetologia 2008;51(8):1399-407. https://doi.org/10.1007/s00125-008-1033-9.
- [32] Rock CL, Thomson C, Gansler T, Gapstur SM, McCullough ML, Patel AV, et al. American Cancer Society guideline for diet and physical activity for cancer prevention. CA Cancer J Clin 2020;70(4):245-71. https://doi.org/10.3322/caac.21591.
- [33] Oppert JM, Bellicha A, van Baak MA, Battista F, Beaulieu K, Blundell JE, Carraça EV, Encantado J, Ermolao A, Pramono A, Farpour-Lambert N, Woodward E, Dicker D, Busetto L. Exercise training in the management of overweight and obesity in adults: Synthesis of the evidence and recommendations from the European Association for the Study of Obesity Physical Activity Working Group. Obes Rev 2021;22 Suppl 4(Suppl 4):e13273. https://doi.org/10.1111/obr.13273.
- [34] Wahrenberg H, Hertel K, Leijonhufvud BM, Persson LG, Toft E, Arner P. Use of waist circumference to predict insulin resistance: retrospective study. BMJ 2005; 330(7504):1363-4. https://doi.org/10.1136/bmj.38429.473310.
- [35] Ramírez-Manent JI, Jover AM, Martinez CS, Tomás-Gil P, Martí-Lliteras P, López-González ÁA. Waist circumference is an essential factor in predicting insulin resistance and early detection of metabolic syndrome in adults. Nutrients 2023;15 (2):257. https://doi.org/10.3390/nu15020257.
- [36] Ross R, Neeland IJ, Yamashita S, Shai I, Seidell J, Magni P, Santos RD, Arsenault B, Cuevas A, Hu FB, Griffin BA, Zambon A, Barter P, Fruchart JC, Eckel RH, Matsuzawa Y, Després JP. Waist circumference as a vital sign in clinical practice: a Consensus Statement from the IAS and ICCR Working Group on Visceral Obesity. Nat Rev Endocrinol 202016(3):177-189. https://doi.org/10.1038/ s41574-019-0310-7.
- [37] Deusdará R, de Moura SA, Szklo M. Association between obesity, overweight, elevated waist circumference, and insulin resistance markers among Brazilian adolescent students. Nutrients 2022;14(17):3487. https://doi.org/10.3390/nu14173487.
- [38] Jiang J, Cai X, Pan Y, Du X, Zhu H, Yang X, et al. Relationship of obesity to adipose tissue insulin resistance. BMJ Open Diabetes Res Care 2020;8(1): e000741.
- [39] Wolfgram PM, Connor EL, Rehm JL, Eickhoff JC, Zha W, Reeder SB, et al. In Nonobese Girls, waist circumference as a predictor of insulin resistance is comparable to MRI fat measures and superior to BMI. Horm Res Paediatr 2015;84 (4):258-65. https://doi.org/10.1159/000439130.
- [40] Lee K. Relationships of neck circumference and abdominal obesity with insulin resistance considering relative handgrip strength in middle-aged and older individuals. Arch Gerontol Geriatrics 2023;114:105097. https://doi.org/ 10.1016/j.archger.2023.105097.
- [41] Han TS, van Leer EM, Seidell JC, Lean ME. Waist circumference action levels in the identification of cardiovascular risk factors: prevalence study in a random sample. BMJ 1995;311(7017):1401-5. https://doi.org/10.1136/ bmj.311.7017.1401.
- [42] Lu Y, Liu S, Qiao Y, Li G, Wu Y, Ke C. Waist-to-height ratio, waist circumference, body mass index, waist divided by height0.5 and the risk of cardiometabolic multimorbidity: A national longitudinal cohort study. Nutr Metab Cardiovasc Dis 2021;31(9):2644-51. https://doi.org/10.1016/j.numecd.2021.05.026.
- [43] Claypool K, Long MT, Patel CJ. Waist circumference and insulin resistance are the most predictive metabolic factors for steatosis and fibrosis. Clin Gastroenterol Hepatol 2023;21(7):1950-1954.e1. https://doi.org/10.1016/j.cgh.2022.05.021.
- [44] Ben-Noun L, Laor A. Relationship of neck circumference to cardiovascular risk factors. Obes Res 2003;11(2):226-31. https://doi.org/10.1038/oby.2003.3.
- [45] Preis SR, Massaro JM, Hoffmann U, D’Agostino Sr RB, Levy D, Robins SJ, et al. Neck circumference as a novel measure of cardiometabolic risk: the Framingham Heart study. J Clin Endocrinol Metab 2010;95(8):3701-10. https://doi.org/ 10.1210/jc.2009-1779.
- [46] Mirr M, Skrypnik D, Bogdanski ´ P, Owecki M. Newly proposed insulin resistance indexes called TyG-NC and TyG-NHtR show efficacy in diagnosing the metabolic syndrome. J Endocrinol Invest 2021;44(12):2831-43. https://doi.org/10.1007/s40618-021-01608-2.
- [47] Brown AE, Walker M. Genetics of insulin resistance and the metabolic syndrome. Curr Cardiol Rep 2016;18:75. https://doi.org/10.1007/s11886-016-0755-4.
- [48] Udler MS, Kim J, von Grotthuss M, Bonàs-Guarch S, Cole JB, Chiou J; Christopher D. Anderson on behalf of METASTROKE and the ISGC; Boehnke M, Laakso M, Atzmon G, Glaser B, Mercader JM, Gaulton K, Flannick J, Getz G, Florez JC. Type 2 diabetes genetic loci informed by multi-trait associations point to disease mechanisms and subtypes: a soft clustering analysis. PLoS Med 2018;15(9): e1002654. https://doi.org/10.1371/journal.pmed.1002654.
- [49] DeForest N,⋅Majithia AR: Genetics of type 2 diabetes: implications from large‑scale studies. Curr Diabetes Rep 2022;22:227-235.
- [50] Williamson A, Norris DM, Yin X, Broadaway KA, Moxley AH, Vadlamudi S, et al. Genome-wide association study and functional characterization identifies candidate genes for insulin-stimulated glucose uptake. Nat Genet 2023;55(6): 973-83. https://doi.org/10.1038/s41588-023-01408-9.
- [51] Sobiczewski W, Wirtwein M, Kowalczys E, Stopczyńska I, Koprowski A, Gruchała M, et al. Heart rate and double product in relation to insulin resistance in patients with hypertension and coronary artery disease. Kardiol Pol 2013;71 (1):47-52.
- [52] Zhou MS, Wang A, Yu H. Link between insulin resistance and hypertension: What is the evidence from evolutionary biology? Diabetol Metab Syndr 2014;6(12): 1-8. https://doi.org/10.1186/1758-5996-6-12.
- [53] Lin CH, Wei JN, Fan KC, Fang CT, Wu WC, Yang CY, et al. Different cutoffs of hypertension, risk of incident diabetes and progression of insulin resistance: A prospective cohort study. J Formos Med Assoc 2022;121(1 Pt 1):193-201. https://doi.org/10.1016/j.jfma.2021.02.022.
- [54] Hall JE, Mouton AJ, da Silva AA, Omoto ACM, Wang Z, Li X, et al. Obesity, kidney dysfunction, and inflammation: interactions in hypertension. Cardiovasc Res 2021;117(8):1859-76. https://doi.org/10.1093/cvr/cvaa336.
- [55] Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28 (7):412-9. https://doi.org/10.1007/BF00280883.
- [56] Soleimani M. Insulin resistance and hypertension: new insights. Kidney Int 2015; 87:497-9. https://doi.org/10.1038/ki.2014.392.
- [57] Stefan N, Cusi K. A global view of the interplay between non-alcoholic fatty liver disease and diabetes. Lancet Diabetes Endocrinol 2022;10(4):284-96. https://doi.org/10.1016/S2213-8587(22)00003-1.
- [58] Stefan N, Schick F, Birkenfeld AL, Häring HU, White MF. The role of hepatokines in NAFLD. Cell Metab 2023;35(2):236-52. https://doi.org/10.1016/j.cmet.2023.01.006.
- [59] Santoro A, Kahn BB: Adipocyte regulation of insulin sensitivity and the risk of type 2 diabetes. N Engl J Med 2023;388(22):2071-2085. https://doi.org/ 10.1056/NEJMra2216691.
- [60] Harlev A, Wiznitzer A. New insights on glucose pathophysiology in gestational diabetes and insulin resistance. Curr Diab Rep 2010;10:242-7. https://doi.org/10.1007/s11892-010-0113-7.
- [61] Gulecoglu Onem MG, Coker C, Baysal K, Altunyurt S, Keskinoglu P. The effects of pre-pregnancy obesity and gestational weight gain on maternal lipid profiles, fatty acids and insulin resistance. J Perinat Med 2021;49(7):873-83. https://doi. org/10.1515/jpm-2020-0540.
- [62] Catalano PM, Kirwan JP, Haugel-de Mouzon S, King J. Gestational diabetes and insulin resistance: role in short- and long-term implications for mother and fetus. J Nutr 2003;133(5 Suppl 2):1674S-83S. https://doi.org/10.1093/jn/133.5.1674S.
- [63] Kotzaeridi G, Blätter J, Eppel D, Rosicky I, Linder T, Geissler F, et al. Characteristics of gestational diabetes subtypes classified by oral glucose tolerance test values. Eur J Clin Invest 2021;51(9):e13628.
- [64] Noctor E, Dunne F. Re: Coustan. Follow-up of women with previous gestational diabetes“ (comment on Noctor et al. ATLANTIC-DIP: prevalence of metabolic syndrome and insulin resistance in women with previous gestational diabetes mellitus by International Association of Diabetes in Pregnancy Study Groups criteria. Acta Diabetol 2015;52:153-160). Acta Diabetol 2016;53(1):135-136.
- [65] Kc K, Shakya S, Zhang H. Gestational diabetes mellitus and macrosomia: a literature review. Ann Nutr Metab 2015;66(Suppl 2):14-20. https://doi.org/10.1159/000371628.
- [66] Lin J, Jin H, Chen L. Associations between insulin resistance and adverse pregnancy outcomes in women with gestational diabetes mellitus: a retrospective study. BMC Pregnancy Childbirth 2021;21(1):526. https://doi.org/10.1186/s12884-021-04006-x.
- [67] Hokanson JE. Hypertriglyceridemia and risk of coronary heart disease. Curr Cardiol Rep 2002;4(6):488-93. https://doi.org/10.1007/s11886-002-0112-7.
- [68] Freeman AM, Pennings N. Insulin resistance. Treasure Island: StatPearls Publishing; 2022.
- [69] von Bibra H, Saha S, Hapfelmeier A, Müller G, Schwarz PEH. Impact of the triglyceride/high-density lipoprotein cholesterol ratio and the hypertriglyceremic-waist phenotype to predict the metabolic syndrome and insulin resistance. Horm Metab Res 2017;49(7):542-9. https://doi.org/10.1055/s-0043-107782.
- [70] Azarpazhooh MR, Najafi F, Darbandi M, Kiarasi S, Oduyemi T, Spence JD. Triglyceride/high-density lipoprotein cholesterol ratio: a clue to metabolic syndrome, insulin resistance, and severe atherosclerosis. Lipids 2021;56(4): 405-12. https://doi.org/10.1002/lipd.12302.
- [71] Alcántara-Alonso E, Molinar-Ramos F, González-López JA, Alcántara-Alonso V, Muñoz-Pérez MA, Lozano-Nuevo JJ, et al. High triglyceride to HDL-cholesterol ratio as a biochemical marker of severe outcomes in COVID-19 patients. Clin Nutr ESPEN 2021;44:437-44. https://doi.org/10.1016/j.clnesp.2021.04.020.
- [72] Bereda G. Dual insulin resistance causes: how frequently type 2 diabetes mellitus and COVID-19 infection caused diabetic ketoacidosis? A case report Ann Med Surg (Lond) 2023;85(4):1096-9. https://doi.org/10.1097/ MS9.0000000000000341.
- [73] Borai A, Livingstone C, Abdelaal F, Bawazeer A, Keti V, Ferns G. The relationship between glycosylated haemoglobin (HbA1c) and measures of insulin resistance across a range of glucose tolerance. Scand J Clin Lab Invest 2011;71(2):168-72. https://doi.org/10.3109/00365513.2010.547947.
- [74] Dubowitz N, Xue W, Long Q, Ownby JG, Olson DE, Barb D, et al. Aging is associated with increased HbA1c levels, independently of glucose levels and insulin resistance, and also with decreased HbA1c diagnostic specificity. Diabet Med 2014;31(8):927-35. https://doi.org/10.1111/dme.12459.
- [75] Saha S, Schwarz PEH. Impact of glycated hemoglobin (HbA1c) on identifying insulin resistance among apparently healthy individuals. J Public Health (Germany) 2017;25(5):505-12. https://doi.org/10.1007/s10389-017-0805-4.
- [76] Osei K, Rhinesmith S, Gaillard T, Schuster D. Is glycosylated hemoglobin A1c a surrogate for metabolic syndrome in nondiabetic, first-degree relatives of African-American patients with type 2 diabetes? J Clin Endocrinol Metab 2003;88(10): 4596-601. https://doi.org/10.1210/jc.2003-030686.
- [77] Boursier G, Sultan A, Molinari N, Maimoun L, Boegner C, Picandet M, et al. Triglycerides and glycated hemoglobin for screening insulin resistance in obese patients. Clin Biochem 2018;53:8-12. https://doi.org/10.1016/j.clinbiochem.2017.12.002.
- [78] Wojcicki JM, Ladyzynski P, Foltynski P, Mikulicz H, Blachowicz J. Tissue insulin sensitivity. Quality factors and performance determinants for successful clamp experiments. Design and development of the TISS system and its clinical verification. Biocybern Biomed Eng 2002;22(2-3):129-44.
- [79] Gower BA, Nagy TR, Goran MI. Visceral fat, insulin sensitivity, and lipids in prepubertal children. Diabetes 1999;48(8):1515-21.
- [80] Saad MF, Anderson RL, Laws A, Watanabe RM, Kades WW, Chen YD, et al. A comparison between the minimal model and the glucose clamp in the assessment of insulin sensitivity across the spectrum of glucose tolerance. Insulin Resistance Atherosclerosis Study Diabetes 1994;43(9):1114-21. https://doi.org/ 10.2337/diab.43.9.1114.
- [81] McAuley KA, Williams SM, Mann JI, Walker RJ, Lewis-Barned NJ, Temple LA, et al. Diagnosing insulin resistance in the general population. Diabetes Care 2001; 24(3):460-4. https://doi.org/10.2337/diacare.24.3.460.
- [82] Raynaud E, Perez-Martin A, Brun JF, Benhaddad AA, Mercier J. Revised concept for the estimation of insulin sensitivity from a single sample. Diabetes Care 1999; 22(6):1003-4. https://doi.org/10.2337/diacare.22.6.1003.
- [83] Duncan MH, Singh BM, Wise PH, Carter G, Alaghband-Zadeh J. A simple measure of insulin resistance. Lancet 1995;346(8967):120-1. https://doi.org/10.1016/s0140-6736(95)92143-5.
- [84] Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care 2004;27(6):1487-95. https://doi.org/10.2337/diacare.27.6.1487.
- [85] Levy JC, Matthews DR, Hermans MP. Correct homeostasis model assessment (HOMA) evaluation uses the computer program. Diabetes Care 1998;21(12): 2191-2. https://doi.org/10.2337/diacare.21.12.2191.
- [86] The Oxford Centre for Diabetes. Endocrinology & Metabolism. HOMA Calculator, https://www.rdm.ox.ac.uk/about/our-clinical-facilities-and-mrc-units/DTU/ software/homa, accessed 2023-05-02.
- [87] University of Oxford. HOMA2 Calculator download, https://www.rdm.ox.ac.uk/about/our-clinical-facilities-and-mrc-units/DTU/software/homa/download, accessed 2023-05-02.
- [88] Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, et al. Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J Clin Endocrinol Metab 2000;85(7): 2402-10. https://doi.org/10.1210/jcem.85.7.6661.
- [89] Yokoyama H, Emoto M, Fujiwara S, Motoyama K, Morioka T, Komatsu M, et al. Quantitative insulin sensitivity check index and the reciprocal index of homeostasis model assessment are useful indexes of insulin resistance in type 2 diabetic patients with wide range of fasting plasma glucose. J Clin Endocrinol Metab 2004;89(3):1481-4. https://doi.org/10.1210/jc.2003-031374.
- [90] Borai A, Livingstone C, Farzal A, Kholeif M, Wang T, Ferns G. Reproducibility of HOMA and QUICKI among individuals with variable glucose tolerance. Diabetes Metab 2010;36(3):247-9. https://doi.org/10.1016/j.diabet.2010.01.006.
- [91] Borai A, Livingstone C, Zarif H, Ferns G. Serum insulin-like growth factor binding protein-1: an improvement over other simple indices of insulin. sensitivity in the assessment of subjects with normal glucose tolerance. Ann Clin Biochem 2009;46 (Pt 2):109-13. https://doi.org/10.1258/acb.2008.008160.
- [92] Matsuda M, DeFronzo RA. Insulin sensitivity indices obtained from oral glucose tolerance testing: Comparison with the euglycemic insulin clamp. Diabetes Care 1999;22(9):1462-70. https://doi.org/10.2337/diacare.22.9.1462.
- [93] Gutch M, Kumar S, Razi SM, Gupta KK, Gupta A. Assessment of insulin sensitivity/resistance. Indian J Endocrinol Metab 2015;19(1):160-4. https://doi. Org/10.4103/2230-8210.146874.
- [94] Peña A, Olson ML, Soltero EG, Lee C, Toledo MJ, Ayers SL, et al. Evaluating a pragmatic estimate of insulin sensitivity in Latino youth with obesity. Clin Obes 2020;10(2):e12353.
- [95] Lorenzo C, Haffner SM, Stančáková A, Kuusisto J, Laakso M. Fasting and OGTTderived measures of insulin resistance as compared with the euglycemic-hyperinsulinemic clamp in nondiabetic Finnish offspring of type 2 diabetic individuals. J Clin Endocrinol Metab 2015;100(2):544-50. https://doi.org/ 10.1210/jc.2014-2299.
- [96] Jayagopal V, Kilpatrick ES, Jennings PE, Hepburn DA, Atkin SL. Biological variation of homeostasis model assessment-derived insulin resistance in type 2 diabetes. Diabetes Care 2002;25(11):2022-5. https://doi.org/10.2337/diacare.25.11.2022.
- [97] Cederholm J, Wibell L. Insulin release and peripheral sensitivity at the oral glucose tolerance test. Diabetes Res Clin Pract 1990;10(2):167-75. https://doi.org/10.1016/0168-8227(90)90040-z.
- [98] Gutt M, Davis CL, Spitzer SB, Llabre MM, Kumar M, Czarnecki EM, et al. Validation of the insulin sensitivity index (ISI(0,120)): comparison with other measures. Diabetes Res Clin Pract 2000;47(3):177-84. https://doi.org/10.1016/s0168-8227(99)00116-3.
- [99] Belfiore F, Iannello S, Volpicelli G. Insulin sensitivity indices calculated from basal and OGTT-induced insulin. glucose. and FFA levels. Mol Genet Metab 1998; 63(2):134-41. https://doi.org/10.1006/mgme.1997.2658.
- [100] Kim JY, Bacha F, Tfayli H, Michaliszyn SF, Yousuf S, Arslanian S. Adipose tissue insulin resistance in youth on the spectrum from normal weight to obese and from normal glucose tolerance to impaired glucose tolerance to type 2 diabetes. Diabetes Care 2019;42(2):265-72. https://doi.org/10.2337/dc18-1178.
- [101] Avignon A, Bœgner C, Mariano-Goulart D, Colette C, Monnier L. Assessment of insulin sensitivity from plasma insulin and glucose in the fasting or post oral glucose-load state. Int J Obes 1999;23(5):512-7. https://doi.org/10.1038/sj.ijo.0800864.
- [102] Stumvoll M, Mitrakou A, Pimenta W, Jenssen T, Yki-Järvinen H, Van Haeften T, et al. Use of the oral glucose tolerance test to assess insulin release and insulin sensitivity. Diabetes Care 2000;23(3):295-301. https://doi.org/10.2337/diacare.23.3.295.
- [103] Stumvoll M, van Haeften T, Fritsche A, Gerich J. Oral Glucose Tolerance Test indexes for insulin sensitivity and secretion based on various availabilities of sampling times. Diabetes Care 2001;24(4):796-7. https://doi.org/10.2337/ diacare.24.4.796.
- [104] Usui I. Hypertension and insulin resistance in adipose tissue. Hypertens Res 2023; 46(6):1478-81. https://doi.org/10.1038/s41440-023-01263-5.
- [105] Guerrero-Romero F, Simental-Mendía LE, González-Ortiz M, Martínez-Abundis E, Ramos-Zavala MG, Hernández-González SO, et al. The product of triglycerides and glucose, a simple measure of insulin sensitivity. Comparison with the euglycemic-hyperinsulinemic clamp. J Clin Endocrinol Metab 2010;95(7): 3347-51. https://doi.org/10.1210/jc.2010-0288.
- [106] Zheng S, Shi S, Ren X, Han T, Li Y, Chen Y, et al. Triglyceride glucose-waist circumference, a novel and effective predictor of diabetes in first-degree relatives of type 2 diabetes patients: cross-sectional and prospective cohort study. J Transl Med 2016;14(1):260. https://doi.org/10.1186/s12967-016-1020-8.
- [107] Kweon S, Kim Y, Jang MJ, Kim Y, Kim K, Choi S, et al. Data resource profile: the Korea National Health and Nutrition Examination Survey (KNHANES). Int J Epidemiol 2014;43(1):69-77. https://doi.org/10.1093/ije/dyt228.
- [108] Zhou M, Zhu L, Cui X, Feng L, Zhao X, He S, et al. The triglyceride to high-density lipoprotein cholesterol (TG/HDL-C) ratio as a predictor of insulin resistance but not of β cell function in a Chinese population with different glucose tolerance status. Lipids Health Dis 2016;15:104. https://doi.org/10.1186/s12944-016-0270-z.
- [109] Bello-Chavolla OY, Almeda-Valdes P, Gomez-Velasco D, Viveros-Ruiz T, Cruz-Bautista I, Romo-Romo A, et al. METS-IR, a novel score to evaluate insulin sensitivity, is predictive of visceral adiposity and incident type 2 diabetes. Eur J Endocrinol 2018;178(5):533-44. https://doi.org/10.1530/EJE-17-0883.
- [110] Guess J, Beltran TH, Choi YS. Prediction of Metabolic Syndrome in U.S. Adults using homeostasis model assessment-insulin resistance. Metab Syndr Relat Disord 2023;21(3):156-62. https://doi.org/10.1089/met.2022.0097.
- [111] Rao K, Yang J, Wu M, Zhang H, Zhao X, Dong Y. Association between the metabolic score for insulin resistance and hypertension in adults: a meta-analysis. Horm Metab Res 2023 Apr;55(4):256-65. https://doi.org/10.1055/a-2010-2452.
- [112] Wu Z, Cui H, Zhang Y, Liu L, Zhang W, Xiong W, et al. The impact of the metabolic score for insulin resistance on cardiovascular disease: a 10-year follow up cohort study. J Endocrinol Invest 2023 Mar;46(3):523-33. https://doi.org/ 10.1007/s40618-022-01925-0.
- [113] Yang W, Cai X, Hu J, Wen W, Mulalibieke H, Yao X, et al. The Metabolic Score for Insulin Resistance (METS-IR) predicts cardiovascular disease and its subtypes in patients with hypertension and obstructive sleep apnea. Clin Epidemiol 2023;15: 177-89. https://doi.org/10.2147/CLEP.S395938.
- [114] Zhang Y, Wang R, Fu X, Song H. Non-insulin-based insulin resistance indexes in predicting severity for coronary artery disease. Diabetol Metab Syndr 2022;14(1): 191. https://doi.org/10.1186/s13098-022-00967-x.
- [115] Paulmichl K, Hatunic M, Højlund K, Jotic A, Krebs M, Mitrakou A, et al. Modification and validation of the triglyceride-to-HDL cholesterol ratio as a surrogate of insulin sensitivity in white juveniles and adults without diabetes mellitus: The single point insulin sensitivity estimator (SPISE). Clin Chem 2016; 62(9):1211-9. https://doi.org/10.1373/clinchem.2016.257436.
- [116] Barchetta I, Dule S, Bertoccini L, Cimini FA, Sentinelli F, Bailetti D, et al. The single-point insulin sensitivity estimator (SPISE) index is a strong predictor of abnormal glucose metabolism in overweight/obese children: a long-term follow-up study. J Endocrinol Invest 2022;45(1):43-51. https://doi.org/10.1007/s40618-021-01612-6.
- [117] Correa-Burrows P, Matamoros M, de Toro V, Zepeda D, Arriaza M, Burrows R. A Single-Point Insulin Sensitivity Estimator (SPISE) of 5.4 is a good predictor of both metabolic syndrome and insulin resistance in adolescents with obesity. Front Endocrinol (Lausanne) 2023;14:1078949. https://doi.org/10.3389/ fendo.2023.1078949.
- [118] Williams KV, Erbey JR, Becker D, Arslanian S, Orchard TJ. Can clinical factors estimate insulin resistance in type 1 diabetes? Diabetes 2000;49(4):626-32. https://doi.org/10.2337/diabetes.49.4.626.
- [119] Pinto C, Sá JR, Lana J, Dualib P, Gabbay M, Dib S. Association of parental cardiovascular risk factors with offspring type 1 diabetes mellitus insulin sensitivity. J Diabetes Complications 2023;37(2):108393. https://doi.org/ 10.1016/j.jdiacomp.2022.108393.
- [120] Zabala A, Darsalia V, Lind M, Svensson AM, Franzén S, Eliasson B, et al. Estimated glucose disposal rate and risk of stroke and mortality in type 2 diabetes: a nationwide cohort study. Cardiovasc Diabetol 2021;20(1):202. https://doi.org/ 10.1186/s12933-021-01394-4.
- [121] Cobb J, Gall W, Adam KP, Nakhle P, Button E, Hathorn J, et al. A novel fasting blood test for insulin resistance and prediabetes. J Diabetes Sci Technol 2013;7 (1):100-10. https://doi.org/10.1177/193229681300700112.
- [122] Kraft J. Detection of diabetes mellitus in situ (occult diabetes). Lab Med 1975;6 (2):10-22.
- [123] Crofts C, Schofield G, Zinn C, Wheldon M, Kraft J. Identifying hyperinsulinaemia in the absence of impaired glucose tolerance: An examination of the Kraft database. Diabetes Res Clin Pract 2016;118:50-7. https://doi.org/10.1016/j. Diabres.2016.06.007.
- [124] Hayashi T, Boyko EJ, Sato KK, McNeely MJ, Leonetti DL, Kahn SE, et al. Patterns of insulin concentration during the OGTT predict the risk of type 2 diabetes in Japanese Americans. Diabetes Care 2013;36(5):1229-35. https://doi.org/10.2337/dc12-0246.
- [125] Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care 2004;27(6):1487-95. https://doi.org/10.2337/diacare.27.6.1487.
- [126] Hoffman RP. Indices of insulin action calculated from fasting glucose and insulin reflect hepatic, not peripheral, insulin sensitivity in African-American and Caucasian adolescents. Pediatr Diabetes 2008;9(3 Pt 2):57-61.
- [127] Szosland K, Lewiński A. In quest for method of insulin resistance assessment in everyday clinical practice-Insulin resistance indices. Diabetes Metab Syndr 2016; 10(1 Suppl 1):S120-5. https://doi.org/10.1016/j.dsx.2015.10.007.
- [128] Tahapary DL, Pratisthita LB, Fitri NA, Marcella C, Wafa S, Kurniawan F, et al. Challenges in the diagnosis of insulin resistance: Focusing on the role of HOMA-IR and Tryglyceride/glucose index. Diabetes Metab Syndr 2022;16(8):102581. https://doi.org/10.1016/j.dsx.2022.102581.
- [129] González-Saldivar G, Rodríguez-Gutiérrez R, Ocampo-Candiani J, González-González JG, Gómez-Flores M. Skin Manifestations of Insulin Resistance: From a Biochemical Stance to a Clinical Diagnosis and Management. Dermatol Ther (Heidelb) 2017;7(1):37-51. https://doi.org/10.1007/s13555-016-0160-3.
- [130] Xing XY, Yang WY, Yang ZJ. The diagnostic significance of homeostasis model assessment of insulin resistance in Metabolic Syndrome among subjects with different glucose tolerance (Chinese). Chin J Diabetes 2004;12(3):182-6.
- [131] Radikova Z, Koska J, Huckova M, Ksinantova L, Imrich R, Vigas M, et al. Insulin sensitivity indices: a proposal of cut-off points for simple identification of insulin-resistant subjects. Exp Clin Endocrinol Diabetes 2006;114(5):249-56. https://doi. org/10.1055/s-2006-924233.
- [132] Szurkowska M, Szafraniec K, Gilis-Januszewska A, Szybiński Z, Huszno B. Insulin resistance indices in population-based study and their predictive value in defining metabolic syndrome. Przegl Epidemiol 2005;59(3):743-51.
- [133] Takahara M, Katakami N, Kaneto H, Noguchi M, Shimomura I. Distribution of the Matsuda Index in Japanese healthy subjects. J Diabetes Investig 2013;4(4): 369-71. https://doi.org/10.1111/jdi.12056.
- [134] Onishi Y, Hayashi T, Sato KK, Leonetti DL, Kahn SE, Fujimoto WY, et al. Comparison of twenty indices of insulin sensitivity in predicting type 2 diabetes in Japanese Americans: The Japanese American Community Diabetes Study. J Diabetes Complications 2020;34(12):107731. https://doi.org/10.1016/j. Jdiacomp.2020.107731.
- [135] Antoniolli LP, Nedel BL, Pazinato TC, de Andrade ML, Gerchman F. Accuracy of insulin resistance indices for metabolic syndrome: a cross-sectional study in adults. Diabetol Metab Syndr 2018;10:65. https://doi.org/10.1186/s13098-018-0365-y.
- [136] Powe CE, Locascio JJ, Gordesky LH, Florez JC, Catalano PM. Oral Glucose Tolerance Test-based measures of insulin secretory response in pregnancy. J Clin Endocrinol Metab 2022;107(5):e1871-8. https://doi.org/10.1210/clinem/dgac041.
- [137] Retnakaran R, Ye C, Hanley AJ, Connelly PW, Sermer M, Zinman B. Subtypes of gestational diabetes and future risk of pre-diabetes or diabetes. EClinicalMedicine 2021;40:101087. https://doi.org/10.1016/j.eclinm.2021.101087.
- [138] Song DK, Hong YS, Sung YA, Lee H. Insulin resistance according to β-cell function in women with polycystic ovary syndrome and normal glucose tolerance. PLoS One 2017;12(5):e0178120.
- [139] Lewandowski K, Głuchowska M, Garnysz K, Horzelski W, Grzesiak M, Lewiński A. High prevalence of early (1st trimester) gestational diabetes mellitus in Polish women is accompanied by marked insulin resistance - comparison to PCOS model. Endokrynol Pol 2022;73(1):1-7. https://doi.org/10.5603/EP. A2021.0095.
- [140] Aizawa T, Nakasone Y, Murai N, Oka R, Nagasaka S, Yamashita K, et al. Hepatic Steatosis and High-Normal Fasting Glucose as Risk Factors for Incident Prediabetes. J Endocr Soc 2022;6. https://doi.org/10.1210/jendso/bvac110.
- [141] Pendharkar SA, Singh RG, Bharmal SH, Drury M, Petrov MS. Pancreatic hormone responses to mixed meal test in new-onset prediabetes/diabetes after non-necrotizing acute pancreatitis. J Clin Gastroenterol 2020;54(2):e11-20. https:// doi.org/10.1097/MCG.0000000000001145.
- [142] Murai N, Saito N, Kodama E, Iida T, Mikura K, Imai H, et al. Association of ghrelin dynamics with beta cell function in Japanese subjects with normal glucose tolerance. Clin Endocrinol 2019;91(5):616-23. https://doi.org/10.1111/cen.14073.
- [143] Bedogni G, Mari A, De Col A, Tamini S, Gastaldelli A, Sartorio A. Association of serum lipids with β-cell function in obese children and adolescents. Endocr Connect 2019;8(10):1318-23. https://doi.org/10.1530/EC-19-0333.
- [144] Otten J, Ahrén B, Olsson T. Surrogate measures of insulin sensitivity vs the hyperinsulinaemic-euglycaemic clamp: a meta-analysis. Diabetologia 2014;57(9): 1781-8. https://doi.org/10.1007/s00125-014-3285-x.
- [145] Pisprasert V, Ingram KH, Lopez-Davila MF, Munoz AJ, Garvey WT. Limitations in the use of indices using glucose and insulin levels to predict insulin sensitivity: impact of race and gender and superiority of the indices derived from oral glucose tolerance test in African Americans. Diabetes Care 2013;36(4):845-53. https://doi.org/10.2337/dc12-0840.
- [146] Song K, Park G, Lee HS, Choi Y, Oh JS, Choi HS, et al. Prediction of insulin resistance by modified triglyceride glucose indices in youth. Life (Basel) 2021;11 (4):286. https://doi.org/10.3390/life11040286.
- [147] Cybulska AM, Schneider-Matyka D, Wieder-Huszla S, Panczyk M, Jurczak A, Grochans E. Diagnostic markers of insulin resistance to discriminate between prediabetes and diabetes in menopausal women. Eur Rev Med Pharmacol Sci 2023;27(6):2453-68. https://doi.org/10.26355/eurrev_202303_31779.
- [148] Hoshino T, Mizuno T, Ishizuka K, Takahashi S, Arai S, Toi S, et al. Triglyceride-glucose index as a prognostic marker after ischemic stroke or transient ischemic attack: a prospective observational study. Cardiovasc Diabetol 2022;21(1):264. https://doi.org/10.1186/s12933-022-01695-2.
- [149] Effoe VS, Wagenknecht LE, Echouffo Tcheugui JB, Chen H, Joseph JJ, Kalyani RR, et al. Sex differences in the association between insulin resistance and incident coronary heart disease and stroke among blacks without diabetes mellitus: the Jackson Heart Study. J Am Heart Assoc 2017;6(2):e004229.
- [150] Schmidt K, Power MC, Ciarleglio A, Nadareishvili Z; IRIS Study Group. Poststroke cognitive impairment and the risk of stroke recurrence and death in patients with insulin resistance. J Stroke Cerebrovasc Dis 2022;31(10):106744.
- [151] Panayiotou AG, Kouis P, Griffin M, Nicolaides AN. Comparison between insulin resistance indices and carotid and femoral atherosclerosis: a cross-sectional population study. Int Angiol 2015;34(5):437-44.
- [152] Erqou S, Adler AI, Challa AA, Fonarow GC, Echouffo-Tcheugui JB. Insulin resistance and incident heart failure: a meta-analysis. Eur J Heart Fail 2022;24(6): 1139-41. https://doi.org/10.1002/ejhf.2531.
- [153] Soares MJ, Calton EK, Pathak K, Zhao Y. Hypothesized pathways for the association of vitamin D status and insulin sensitivity with resting energy expenditure: a cross sectional mediation analysis in Australian adults of European ancestry. Eur J Clin Nutr 2022;76(10):1457-63. https://doi.org/10.1038/ s41430-022-01123-4109.
- [154] Li H, Xie X, Bai G, Qiang D, Zhang L, Liu H, et al. Vitamin D deficiency leads to the abnormal activation of the complement system. Immunol Res 2023;71(1):29-38. https://doi.org/10.1007/s12026-022-09324-6.
- [155] Xu Z, Gong R, Luo G, Wang M, Li D, Chen Y, et al. Association between vitamin D3 levels and insulin resistance: a large sample cross-sectional study. Sci Rep 2022; 12(1):119. https://doi.org/10.1038/s41598-021-04109-7.
- [156] Moshkovits Y, Rott D, Chetrit A, Dankner R. The insulin sensitivity McAuley index (MCAi) is associated with 40-year cancer mortality in a cohort of men and women free of diabetes at baseline. PLoS One 2022;17(8):e0272437.
- [157] Dinh Le T, Minh Bui T, Hien VT, Phi Thi Nguyen N, Thanh Thi Tran H, Nguyen ST, et al. Insulin resistance in gestational diabetes mellitus and its association with anthropometric fetal indices. Clin Med Insights Endocrinol. Diabetes 2022;15. https://doi.org/10.1177/11795514221098403.
- [158] Garg MK, Tandon N, Marwaha RK, Singh Y. Evaluation of surrogate markers for insulin resistance for defining metabolic syndrome in urban Indian adolescents. Indian Pediatr 2014;51(4):279-84. https://doi.org/10.1007/s13312-014-0401-4.
- [159] Tripathy D, Cobb JE, Gall W, Adam KP, George T, Schwenke DC, et al. A novel insulin resistance index to monitor changes in insulin sensitivity and glucose tolerance: the ACT NOW study. J Clin Endocrinol Metab 2015;100(5):1855-62. https://doi.org/10.1210/jc.2014-3824.
- [160] Derosa G, Maffioli P, Salvadeo SA, Ferrari I, Gravina A, Mereu R, et al. Direct comparison among oral hypoglycemic agents and their association with insulin resistance evaluated by euglycemic hyperinsulinemic clamp: the 60’s study. Metabolism 2009;58(8):1059-66. https://doi.org/10.1016/j. Metabol.2009.03.007.
- [161] Zheng D, Dou J, Liu G, Pan Y, Yan Y, Liu F, et al. Association between triglyceride level and glycemic control among insulin-treated patients with type 2 diabetes. J Clin Endocrinol Metab 2019;104(4):1211-20. https://doi.org/10.1210/jc.2018-01656.
Typ dokumentu
Bibliografia
Identyfikator YADDA
bwmeta1.element.baztech-ce5ec44b-54fa-4924-a30e-8bc0750d2ab7