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Insulin resistance and hypersecretion in obesity: European Group for the Study of Insulin Resistance (EGIR)
Open accessAbstract
Insulin resistance and insulin hypersecretion are established features of obesity. Their prevalence, however, has only been inferred from plasma insulin concentrations. We measured insulin sensitivity (as the whole-body insulin-mediated glucose uptake) and fasting posthepatic insulin delivery rate (IDR) with the use of the euglycemic insulin clamp technique in a large group of obese subjects in the database of the European Group for the Study of Insulin Resistance (1,146 nondiabetic, normotensive Caucasian men and women aged 18-85 yr, with a body mass index (BMI) ranging from 15 to 55 kg.m-2). Insulin resistance, defined as the lowest decile of insulin sensitivity in the lean subgroup (608 subjects with a mean BMI of 29 kg.m-2). Insulin sensitivity declined linearly with BMI at an age- and sex-adjusted rate of 1.2 micromol.min-1.kg FFM-1 per BMI unit (95% confidence intervals = 1.0-1.4). Insulin hypersecretion, defined as the upper decile of IDR, was significantly (P<0.0001) more prevalent (38%) than insulin resistance in the obese group. In the whole dataset, IDR rose as a function of both BMI and insulin resistance in a nonlinear fashion. Neither the waist circumference nor the waist-to-hip ratio, indices of body fat distribution, was related to insulin sensitivity after adjustment for age, gender, and BMI; both, however, were positively associated (P<0.001) with insulin hypersecretion, particularly in women. In nondiabetic, normotensive obese subjects, the prevalence of insulin resistance is relatively low, and is exceeded by the prevalence of insulin hypersecretion, particularly in women with central obesity. In the obese with preserved insulin sensitivity, risk for diabetes, cardiovascular risk, and response to treatment may be different than in insulin resistant obesity.
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“Because the great majority of glucose disposal after intravenous glucose administration occurs in muscle, these results provide strong evidence that insulin resistance in muscle is the earliest demonstrable defect in the natural history of type 2 diabetes, but that the development of overt type 2 diabetes occurs only in those individuals whose β-cells are unable to compensate for the defect in”
From Skeletal Muscle Insulin Resistance Is the Primary Defect in Type 2 Diabetes (2009) · cites this paper as [48]
Experimental — accuracy not yet measuredIn the citing paper
“Given the strong association between BMI and insulin sensitivity (8), groups with large differences in insulin sensitivity are generally difficult to match for BMI and fat mass, complicating data interpretation.”
From Metabolic flexibility to lipid availability during exercise is enhanced in individuals with high insulin sensitivity (2018) · cites this paper as [8]
In the citing paper
“A similar relationship also exists between BMI and the degree of insulin resistance.22”
From A review of current trends with type 2 diabetes epidemiology, aetiology, pathogenesis, treatments and future perspectives (2021) · cites this paper as [22]
In the citing paper
“one study reported that 19, 34 and 60% of individuals with a BMI of <30, ≥30–35 and >35, respectively, were insulin resistant.22”
From A review of current trends with type 2 diabetes epidemiology, aetiology, pathogenesis, treatments and future perspectives (2021) · cites this paper as [22]
In the citing paper
“It is well established that there is a generally directly proportional relationship between BMI and both fasting and postprandial insulin levels.21,22”
From A review of current trends with type 2 diabetes epidemiology, aetiology, pathogenesis, treatments and future perspectives (2021) · cites this paper as [22]
In the citing paper
“The hyperinsulinemia associated with rising BMI is necessary to overcome insulin resistance and maintain normoglycemia.22”
From A review of current trends with type 2 diabetes epidemiology, aetiology, pathogenesis, treatments and future perspectives (2021) · cites this paper as [22]
In the citing paper
“Insulin hypersecretion also becomes more frequent with increasing BMI;24 28, 49 and 80% of individuals with a BMI of <30, >30–35 and >35, respectively, exhibited insulin hypersecretion.22”
From A review of current trends with type 2 diabetes epidemiology, aetiology, pathogenesis, treatments and future perspectives (2021) · cites this paper as [22]
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“Further, if the insulin sensitivity index (ISI) were calculated as the ratio of ‘‘M’’ to fasting insulin (16), there would be further separation of the group data.”
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“the Genetic Architecture of Fasting Glucose and Insulin Ching-Ti Liu,1,84,* Sridharan Raghavan,2,3,4,84 Nisa Maruthur,5,6,7,84 Edmond Kato Kabagambe,8,84 Jaeyoung Hong,1 Maggie C.Y. Ng,9,10 Marie-France Hivert,11,12,13 Yingchang Lu,14,15 Ping An,16 Amy R. Bentley,17 Anne M. Drolet,18 Kyle J. Gaulton,19 Xiuqing Guo,20…”
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Kopp, W. (2003) · Metabolism · doi:10.1016/s0026-0495(02)05294-0 · Cited by 51
Polycystic Ovary Syndrome, Insulin Resistance, and Molecular Defects of Insulin Signaling
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Creatine supplementation alters insulin secretion and glucose homeostasis in vivo
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“[12] BMI, though used as a simple mean to define obesity, does not actually demarcate between fatty and fat‐free mass[13] and do not give any qualitative inference.”
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“(Ferrannini et al., 1997) This has led to the concept of metabolically healthy obesity (MHO), which is defined as obesity in the absence of metabolic syndrome.”
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Low 25‐Hydroxyvitamin D Does Not Affect Insulin Sensitivity in Obesity after Bariatric Surgery
Manco, M., Calvani, M., Nanni, G., Greco, A. V., Iaconelli, A., Gasbarrini, A., Castagneto, M., & Mingrone, G. (2005) · Obesity Research · doi:10.1038/oby.2005.207 · Cited by 49
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“In previous studies, higher body mass index was found to be related with insulin resistance with or without other associated conditions [30,31,32].”
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Reinehr, T., Holl, R. W., Roth, C. L., Wiesel, T., Stachow, R., Wabitsch, M., Andler, W., & on behalf of the DPV-Wiss Study Group (2005) · Pediatric Diabetes · doi:10.1111/j.1399-543x.2005.00093.x · Cited by 49
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“Overweight or obesity also results in a tremendous fall in insulin sensitivity, combined with a markedly increased risk for type 2 diabetes and other disturbances (such as hyperlipidemia or arterial hypertension) (1,7).”
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Geluk, C. A., Asselbergs, F. W., Hillege, H. L., Bakker, S. J. L., de Jong, P. E., Zijlstra, F., & van Gilst, W. H. (2005) · European Heart Journal · doi:10.1093/eurheartj/ehi253 · Cited by 48
Jensterle, M., Janez, A., Mlinar, B., Marc, J., Prezelj, J., & Pfeifer, M. (2008) · European Journal of Endocrinology · doi:10.1530/eje-07-0857 · Cited by 47
Effects of Bariatric Surgery on Early Myocardial Alterations in Adult Severely Obese Subjects
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Ferrannini, E., Gastaldelli, A., Matsuda, M., Miyazaki, Y., Pettiti, M., Glass, L., & DeFronzo, R. A. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021864 · Cited by 46
“Furthermore, we have previously shown that WHR increases linearly with BMI in the low range (below 28 kg/m(2)) and levels off in the obese range (22).”
BackgroundSelf-citationAbdominal and gynoid adipose distribution and incident myocardial infarction in women and men
Wiklund, P. N., Toss, F., Jansson, J.-H., Eliasson, M., Hallmans, G., Nordström, A., Franks, P. W., & Nordström, P. (2010) · International Journal of Obesity · doi:10.1038/ijo.2010.102 · Cited by 46
First-phase insulin secretion: can its evaluation direct therapeutic approaches?
Di Giuseppe, G., Ciccarelli, G., Soldovieri, L., Capece, U., Cefalo, C. M. A., Moffa, S., Nista, E. C., Brunetti, M., Cinti, F., Gasbarrini, A., et al. (2023) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2023.02.001 · Cited by 46
Hyperinsulinemia in individuals with obesity: Role of insulin clearance
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“There is general agreement (1-3) that hyperinsulinemia in individuals with obesity is related to increases in insulin secretion and decreases in insulin clearance rate (ICR).”
BackgroundInfluentialInsulin-sensitive obese children display a favorable metabolic profile
Vuković, R., Mitrović, K., Milenković, T., Todorovic, S., Soldatović, I., Grujičić, S. Š., & Zdravković, D. (2012) · European Journal of Pediatrics · doi:10.1007/s00431-012-1867-5 · Cited by 46
Differential Intra-abdominal Adipose Tissue Profiling in Obese, Insulin-resistant Women
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“The association between obesity and insulin resistance was described many years ago [1, 2].”
BackgroundPathophysiology of diabetes mellitus type 2: beyond the duo "insulin resistance-secretion deficit".
Boada, C. A. C., & Martínez-Moreno, J. M. (2013) · PubMed · doi:10.3305/nh.2013.28.sup2.6717 · Cited by 44
Merino, B., Fernández-Díaz, C. M., Parrado‐Fernández, C., González-Casimiro, C. M., Postigo, T., Lobatón, C. D., Leissring, M. A., Cózar‐Castellano, I., & Perdomo, G. (2020) · Metabolism · doi:10.1016/j.metabol.2020.154352 · Cited by 46
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“In work done by Ferrannini et al [35], it was recognised that although insulin hypersecretion can occur in adults with uncomplicated obesity, the prevalence of insulin resistance is low.”
Effects of Growth Hormone Treatment in Obese Prepubertal Boys1
Kamel, A. F., Norgren, S., Elimam, A., Danielsson, P., & Marcus, C. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.4.6492 · Cited by 46
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Baratta, R., Paola, R. D., Spampinato, D., Fini, G., Marucci, A., Coco, A., Vigneri, R., Frittitta, L., & Trischitta, V. (2003) · Journal of Molecular Medicine · doi:10.1007/s00109-003-0466-3 · Cited by 46
Obesity, free fatty acids, and insulin resistance
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Cirurgia bariátrica cura síndrome metabólica?
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“While the Euglycemic Hyperinsulinemic Clamp (EHC) has been long considered as the “golden standard” in clinical research [10], it requires careful training of the operator, and may be potentially dangerous for the subjects investigated due to the high levels of insulinemia reached * Correspondence: simona.”
BackgroundSelf-citationRisks of Coronary Heart Disease in Women: Current Understanding and Evolving Concepts
Tsang, T. S. M., Barnes, M. E., Gersh, B. J., & Hayes, S. N. (2000) · Mayo Clinic Proceedings · doi:10.4065/75.12.1289 · Cited by 45
Inhibitor κB kinase is involved in the paracrine crosstalk between human fat and muscle cells
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“Furthermore, we did not observe any major difference in variables linked to insulin resistance between these two control groups, consistent with the known overlap in insulin sensitivity between lean control subjects and obese nondiabetic subjects (19).”
ResultRetractedAssessment of insulin resistance in young women with polycystic ovary syndrome
Jensterle, M., Weber, M. M., Pfeifer, M., Preželj, J., Pfützner, A., & Janež, A. (2008) · International Journal of Gynecology & Obstetrics · doi:10.1016/j.ijgo.2008.03.017 · Cited by 43
“International Federation ofGynecol PCOS [2,4] whereas its prevalence in the general population is between 10% and 25% [5,6], depending on method of assessment and mean body weight.”
MethodTargets to treat metabolic syndrome in polycystic ovary syndrome
Mahalingaiah, S., & Diamanti‐Kandarakis, E. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2015.1101067 · Cited by 44
“However, certain phenotypes are associated with insulin resistance and an increased long-term risk of developing diabetes,[6,7] metabolic syndrome (MBS),[8,9] and cardiovascular disease,[10,11] which are compounded by concurrent obesity.[12,13]”
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Utzschneider, K. M., de Lagemaat, A. V., Faulenbach, M. V., Goedecke, J. H., Carr, D. B., Boyko, E. J., Fujimoto, W. Y., & Kahn, S. E. (2010) · Obesity · doi:10.1038/oby.2010.77 · Cited by 43
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“This issue is important because obesity has been implicated to increase insulin secretion (13,28,29).”
BackgroundIntra-abdominal adiposity, abdominal obesity, and cardiometabolic risk
Ferrannini, E., Sironi, A. M., Iozzo, P., & Gastaldelli, A. (2008) · European Heart Journal Supplements · doi:10.1093/eurheartj/sum042 · Cited by 43
“This is because the expanded mass of all adipose depots—VAT as well as SAT (Figure 7)—provides an additional reservoir for insulin-mediated glucose uptake despite the insulin resistance.(22) Figure 10 Relationship between insulin-mediated glucose uptake (by (18)FDG positron emitting tomography scan) and blood flow (by…”
BackgroundSelf-citationModification of Insulin, Glucose and Cholesterol Levels in Nonobese Women Undergoing Liposuction
Robles‐Cervantes, J. A., az, S. Y. N.-D., & Cárdenas-Camarena, L. (2003) · Annals of Plastic Surgery · doi:10.1097/01.sap.0000096448.59407.43 · Cited by 43
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Insulin Clearance in Obesity and Type 2 Diabetes
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The Insulin Tolerance Test in Morbidly Obese Patients Undergoing Bariatric Surgery
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Obesity-related insulin resistance: implications for the surgical patient
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Mediating Effects of Inflammatory Biomarkers on Insulin Resistance Associated with Obesity
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“The following approach was used, which was based on standard linear methods on insulin kinetics and was previously used by others (13) to calculate posthepatic insulin delivery (RSYS in our model):”
MethodInsulin resistance and muscle wasting in non-diabetic end-stage renal disease patients
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“Obesity is another example of IR state [44,45] and weight loss resulted in the improvement of insulin sensitivity [46].”
BackgroundObesity Affects Myocardial Vasoreactivity and Coronary Flow Response to Insulin
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“Moreover, obesity itself has been associated with increased insulin secretion [31], decreased insulin clearance [32], and increased insulin resistance.”
BackgroundHyperinsulinemia: an early biomarker of metabolic dysfunction
Vaidya, R. A., Desai, S., Moitra, P., Salis, S. S., Agashe, S., Battalwar, R., Mehta, A., Madan, J., Kalita, S., Udipi, S. A., et al. (2023) · Frontiers in Clinical Diabetes and Healthcare · doi:10.3389/fcdhc.2023.1159664 · Cited by 45
“Hypersecretion of insulin and hyperinsulinemia could occur prior to insulin resistance and contribute not only to T2D but also the risk of CVD (23, 24).”
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“Previous studies have shown that hyperinsulinemia in individuals with obesity is related to increases in insulin secretion and decreases in insulin clearance (2-4).”
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BackgroundImpact of Postprandial Hypoglycemia on Weight Loss After Bariatric Surgery
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Self-citationThe Metabolically Healthy But Obese Phenotype in African Americans
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Insulin, renin-aldosterone system and blood pressure in obese people
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“Insulin resistance is associated with numerous diseases including obesity, metabolic syndrome, and type 2 diabetes mellitus (39).”
BackgroundPolycystic ovary syndrome. Revised diagnostic criteria and long-term health consequences
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Metadata
- Authors
- Ferrannini, E., Natali, A., Bell, P., Cavallo-Perin, P., Lalic, N., & Mingrone, G.
- Affiliations
- Istituto di Fisiologia Clinica (IT)
- Venue
- Journal of Clinical Investigation
- Published
- 1997-09-01
- Volume
- 100
- Issue
- 5
- Pages
- 1166-1173
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC508292
- OpenAlex
- W2036400933
- Cited by
- 898
- References
- 53
- Citations by year
- 2026: 9 · 2025: 14 · 2024: 20 · 2023: 13 · 2022: 20 · 2021: 28 · 2020: 32 · 2019: 26 · 2018: 32 · 2017: 26 · 2016: 26 · 2015: 36 · 2014: 30 · 2013: 36 · 2012: 43
- FWCI
- 10.82
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CINECA IRIS Institutial research information system (University of Pisa) (submittedVersion)
- Funders
- Università degli Studi di Napoli Federico II
- Helsingin Yliopisto
- Universität Heidelberg
- Lunds Universitet
- Università degli Studi di Padova
- National and Kapodistrian University of Athens
- Université de Genève
- Università degli Studi di Torino
- Università degli Studi di Verona
- Topics
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Pancreatic function and diabetes
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- insulin resistance, insulin hypersecretion, obesity, insulin sensitivity, body mass index, waist circumference, waist-to-hip ratio, abdominal obesity, sex differences, hyperinsulinemic-euglycemic clamp, type 2 diabetes risk
- MeSH terms
- Insulin Secretion, Adolescent, Adult, Aged, Aged, 80 and over, Female, Humans, Insulin, Insulin Resistance, Male, Middle Aged, Obesity, Body Mass Index
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