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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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In the citing paper
“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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“Furthermore, this fat mass showed a positive correlation with the glucose-induced insulin response in rats on HF diet, which corresponds to findings in obese subjects in which body fat mass correlates positively with glucose-stimulated insulin secretion”
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“In obese individuals without T2DM, insulin hypersecretion and hyperinsulinemia are more prevalent than insulin resistance, indicating that hyperinsulinemia may precede and/or exacerbate insulin resistance [56,57].”
BackgroundPrevalence and Clinical Profile of Metabolic Obesity and Phenotypic Obesity in Asian Indians
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Relationship between changes in neck circumference and changes in blood pressure
Ben-Noun, L. L. (2004) · American Journal of Hypertension · doi:10.1016/j.amjhyper.2004.02.005 · Cited by 72
Reappraising the relationship between hyperinsulinemia and insulin resistance in PCOS
Houston, E. J., & Templeman, N. M. (2025) · Journal of Endocrinology · doi:10.1530/joe-24-0269 · Cited by 93
Nadler, E. P., Reddy, S., Isenalumhe, A., Youn, H. A., Peck, V., Ren, C. J., & Fielding, G. (2009) · Journal of the American College of Surgeons · doi:10.1016/j.jamcollsurg.2009.07.022 · Cited by 71
McLaughlin, T., Abbasi, F., Carantoni, M., Schaaf, P., & Reaven, G. M. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.2.5441 · Cited by 75
Ferrannini, E., Iozzo, P., Virtanen, K. A., Honka, M., Bucci, M., & Nuutila, P. (2018) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy162 · Cited by 73
Self-citationBruehl, H., Sweat, V., Hassenstab, J. J., Polyakov, V., & Convit, A. J. (2009) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803390903224928 · Cited by 69
“Insulin resistance (IR), which is considered to be etiologically linked to obesity (Ferrannini et al., 1997), is an early phenomenon in the course of developing T2DM and is characterized by high circulating fasting insulin levels with fasting glucose levels still within the normal range (Sesti,…”
BackgroundCostes, S., Bertrand, G., & Ravier, M. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105303 · Cited by 77
Central Nervous System Control of Glucose Homeostasis: A Therapeutic Target for Type 2 Diabetes?
Mirzadeh, Z., Faber, C. L., & Schwartz, M. W. (2022) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-052220-010446 · Cited by 73
Wiklund, P., Zhang, X., Pekkala, S., Autio, R., Kong, L., Yang, Y., Keinanen-Kiukaanniemi, S. M., Alén, M., & Cheng, S. (2016) · Scientific Reports · doi:10.1038/srep24540 · Cited by 68
Relationship between impaired glucose tolerance, non‐insulin‐dependent diabetes mellitus and obesity
Ferrannini, & Camastra, S. (1998) · European Journal of Clinical Investigation · doi:10.1046/j.1365-2362.1998.0280s2003.x · Cited by 68
Mechanisms Underlying Type 2 Diabetes Remission After Metabolic Surgery
Pérez‐Pevida, B., Escalada, J., Miras, A. D., & Frühbeck, G. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00641 · Cited by 68
“For instance, a 30% reduction in body mass index predicts a 50% increase in insulin sensitivity as seen in the European Group for the Study of Insulin Resistance (EGIR) cohort among others (19, 39, 46).”
BackgroundMcLaughlin, T., Deng, A. C., Gonzales, O., Aillaud, M., Yee, G., Lamendola, C. A., Abbasi, F., Connolly, A. J., Sherman, A., Cushman, S. W., et al. (2008) · Diabetologia · doi:10.1007/s00125-008-1148-z · Cited by 68
Polycystic ovary syndrome (PCOS)
Dewailly, D., Hiéronimus, S., Mirakian, P., & Hugues, J. (2010) · Annales d Endocrinologie · doi:10.1016/j.ando.2009.12.003 · Cited by 67
Predictors of the metabolic syndrome and correlation with computed axial tomography
González, A. S., Bellido, D., Buño, M., Pértega-Díaz, S., de Luis, D. A., Olmos, M. Á. M., & Vidal, O. (2006) · Nutrition · doi:10.1016/j.nut.2006.08.019 · Cited by 67
“However, the superirity of waist circumference as a clinical tool should be uestioned, as reported by the European Group for the tudy of Insulin Resistance [7], which showed that the agnitude of the correlation between insulin resistance and besity does not increase when the waist/hip ratio is relaced by BMI as a mark…”
Methodter Horst, K. W., Gilijamse, P. W., de Weijer, B. A., Kiliçarslan, M., Ackermans, M. T., Nederveen, A. J., Nieuwdorp, M., Romijn, J. A., & Serlie, M. J. M. (2015) · Frontiers in Endocrinology · doi:10.3389/fendo.2015.00182 · Cited by 70
“Few studies have investigated insulin sensitivity in matched severely obese men and women, who are exceptionally prone to develop insulin resistance (26), or described gender differences in tissue-specificmeasurements of insulin sensitivity in liver and adipose tissue of men and women.”
BackgroundMoran, L. J., Noakes, M., Clifton, P. M., Wittert, G. A., Belobrajdic, D. P., & Norman, R. J. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-2336 · Cited by 66
“Waist circumference does not distinguish between the relative proportions of sc and visceral abdominal adipose tissue and was not associated with insulin sensitivity assessed by euglycemic hyperinsulinemic clamp in the European Group for the Study of IR (50).”
BackgroundZawalich, W. S., & Zawalich, K. C. (2000) · Endocrinology · doi:10.1210/endo.141.9.7636 · Cited by 70
Predictors of weight loss and reversal of comorbidities in malabsorptive bariatric surgery
Mora, M. E. V., Simeoni, B., Gagliardi, L., Scarfone, A., Nanni, G., Castagneto, M., Manco, M., Mingrone, G., & Ferrannini, E. (2005) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/81.6.1292 · Cited by 65
Self-citationInsulin resistance in obesity can be reliably identified from fasting plasma insulin
ter Horst, K. W., Gilijamse, P. W., Koopman, K. E., de Weijer, B. A., Brands, M., Kootte, R. S., Romijn, J. A., Ackermans, M. T., Nieuwdorp, M., Soeters, M. R., et al. (2015) · International Journal of Obesity · doi:10.1038/ijo.2015.125 · Cited by 65
Genetics of Obesity and Type 2 Diabetes
Bougneres, P. F. (2002) · Diabetes · doi:10.2337/diabetes.51.2007.s295 · Cited by 66
Larsson, H. E., & Åhrén, B. (2000) · Diabetologia · doi:10.1007/s001250050029 · Cited by 65
Svendsen, P. F., Nilas, L., Madsbad, S., & Holst, J. J. (2009) · Metabolism · doi:10.1016/j.metabol.2008.11.009 · Cited by 64
“There has been some debate about the effect of obesity on the incretin effect [10-16].”
BackgroundSardinha, L. B., Teixeira, P. J., Guedes, D. P., Going, S. B., & Lohman, T. G. (2000) · Metabolism · doi:10.1053/meta.2000.17716 · Cited by 64
Subcutaneous adipose tissue accumulation protects systemic glucose tolerance and muscle metabolism
Booth, A. D., Magnuson, A. M., Fouts, J. K., Wei, Y., Wang, D., Pagliassotti, M. J., & Foster, M. T. (2018) · Adipocyte · doi:10.1080/21623945.2018.1525252 · Cited by 61
Chen, W., Pan, Y., Jing, J., Zhao, X., Liu, L., Meng, X., Wang, Y., Wang, Y., Johnston, S. C., Wang, Z., et al. (2017) · Journal of the American Heart Association · doi:10.1161/jaha.116.005446 · Cited by 60
“Furthermore, the association between obesity and insulin resistance was similar regardless of whether WC or BMI was used for obesity diagnosis.(32) Using METS with the IDF definition in a sensitivity analysis in our study, the results also demonstrated similar results.”
ResultInsulin resistance, dyslipidemia, and metabolic syndrome in women with polycystic ovary syndrome
El-Mazny, A. N., Abou-Salem, N. A., El-Sherbiny, W. S., & El-Mazny, A. (2010) · International Journal of Gynecology & Obstetrics · doi:10.1016/j.ijgo.2010.01.014 · Cited by 61
Association between weight fluctuation and fasting insulin concentration in Japanese men
Yatsuya, H., Tamakoshi, K., Yoshida, T., Hori, Y., Zhang, H., Ishikawa, M., Zhu, S., Kondo, T., & Toyoshima, H. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802221 · Cited by 60
Sung, K., Ryan, M. C., Kim, B. S., Cho, Y. K., Kim, B. I., & Reaven, G. M. (2007) · Diabetes Care · doi:10.2337/dc07-0512 · Cited by 60
Park, S. H., Kim, B. I., Kim, S. H., Kim, H. J., Park, D. I., Cho, Y. K., Sung, I. K., Sohn, C. I., Kim, H. Y., Keum, D. K., et al. (2007) · Journal of the American College of Nutrition · doi:10.1080/07315724.2007.10719618 · Cited by 59
“According to the European Group for the Study of Insulin Resistance, only 26% of obese individuals exhibit insulin resistance [10].”
MethodTransamination Is Required for α-Ketoisocaproate but Not Leucine to Stimulate Insulin Secretion*
Zhou, Y., Jetton, T. L., Goshorn, S., Lynch, C. J., & She, P. (2010) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.136846 · Cited by 60
Masharani, U. B., Maddux, B. A., Li, X., Sakkas, G. K., Mulligan, K. M., Schambelan, M., Goldfine, I. D., & YOUNGREN, J. F. (2011) · PLoS ONE · doi:10.1371/journal.pone.0019878 · Cited by 62
“in skeletal muscle [3–5], so much of the work exploring the”
Backgroundfor the EGIR-RISC Study Group, Tricò, D., Mengozzi, A., Nesti, L., Hatunic, M., Sánchez, R. G., Konrad, T., Lalic, K. S., Lalic, N. M., Mari, A., et al. (2019) · Diabetologia · doi:10.1007/s00125-019-05013-6 · Cited by 59
“Still, differences in palmitoleate enrichment might aid understanding of the wide inter-individual variability in the negative impact of obesity on glucose metabolism [50].”
BackgroundSelf-citationBrain control of blood glucose levels: implications for the pathogenesis of type 2 diabetes
Alonge, K. M., D’Alessio, D. A., & Schwartz, M. W. (2020) · Diabetologia · doi:10.1007/s00125-020-05293-3 · Cited by 62
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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