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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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Tousignant, B., Faraj, M., Conus, F., Garrel, D. R., Brochu, M., RABASA-LHORET, R. P. R., & Coderre, L. (2008) · International Journal of Obesity · doi:10.1038/ijo.2008.163 · Cited by 14
Klement, J., Kubera, B., Eggeling, J., Rädel, C., Wagner, C., Park, S. Q., & Peters, A. (2018) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2018.01.014 · Cited by 14
Pereira, J. A., Claro, B. M., Pareja, J. C., Chaim, É. A., Astiarraga, B., Saad, M. J. A., & Muscelli, E. (2003) · International Journal of Obesity · doi:10.1038/sj.ijo.0802269 · Cited by 14
Pathogenesis of type 2 diabetes mellitus
DeFronzo, R. A. (2015) · Wiley eBooks · doi:10.1002/9781118387658.ch25 · Cited by 17
Predictors of insulin resistance in the obese with metabolic syndrome
Manu, P., Tsang, J. C., Napolitano, B. A., LESSER, M. L., & Correll, C. U. (2010) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2010.05.015 · Cited by 13
Kim, M. K., Jang, E., Son, J. W., Kwon, H.-S., Baek, K., Lee, K., & Song, K. (2011) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2011.04.009 · Cited by 14
“In fact, data from the European Group for the Study of Insulin Resistance suggest that about 25% of obese individuals (BMI > 35 kg/m) are insulin sensitive [10].”
BackgroundThe status of diabetes and its complications in Latin-American population: A review article
Correa, R. R., Tella, S. H., Elshimy, G., & Davidson, J. A. (2020) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2020.108274 · Cited by 14
“clamp technique studies have shown that obesity leads to insulin resistance at liver, muscle and adipose tissue [36,37].”
BackgroundBoyer, W. R., Johnson, T. M., Fitzhugh, E. C., Richardson, M. R., & Churilla, J. R. (2016) · Metabolic Syndrome and Related Disorders · doi:10.1089/met.2015.0077 · Cited by 13
“Furthermore, studies have also shown that not all obese subjects have IR 8–10 and not all subjects with desirable adiposity levels are insulin sensitive.”
Ferrannini, E., Moreira, R. P., Seghieri, M., Rebelos, E., de Souza, A. L., Chueire, V. B., Arvia, C., & Muscelli, E. (2020) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2020-001178 · Cited by 13
Self-citationGlucose uptake saturation explains glucose kinetics profiles measured by different tests
Bizzotto, R., Natali, A., Gastaldelli, A., Muscelli, E., Krššák, M., Brehm, A., Roden, M., Ferrannini, E., & Mari, A. (2016) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00045.2016 · Cited by 13
“The expected negative correlation was reproduced, in accord with previous analyses on insulin sensitivity (17), and was homogeneous across all studies.”
ResultSelf-citationInsulin resistance and β‐cell dysfunction as therapeutic targets in type 2 diabetes
Evans, A. J., & Krentz, A. J. (2001) · Diabetes Obesity and Metabolism · doi:10.1046/j.1463-1326.2001.00101.x · Cited by 13
Serum Adiponectin in Alzheimer’s Disease (AD): Association with AD Biomarkers and Cognitive Outcome
Kim, H., Initiative, A. D. N., Jun, S., Kim, B. S., & Kim, I.-J. (2021) · Journal of Alzheimer s Disease · doi:10.3233/jad-210722 · Cited by 11
Kim, Y., Son, T., Park, J., Jun, W., & Kim, O. (2022) · Molecular Nutrition & Food Research · doi:10.1002/mnfr.202200358 · Cited by 13
Isidoro, B., Lope, V., Pedraz‐Pingarrón, C., Collado-García, F., Santamariña, C., Moreo, P., Vidal, C., Laso, M. S., García‐López, M., & Pollán, M. (2011) · BMC Public Health · doi:10.1186/1471-2458-11-960 · Cited by 12
“Obesity is a known risk factor for many chronic diseases [26-28], including breast cancer among post-menopausal women [29].”
BackgroundStrack, C., Baessler, A., Wagner, F. M., Bruxmeier, J., Yaroslavskyy, O., Rousseva, E., Loew, T. H., Riegger, G. A. J., Schmitz, G., & Fischer, M. (2012) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.10918 · Cited by 12
Hurwitz, B. E., Schneiderman, N., Marks, J. B., Mendez, A. J., Gonzalez, A., Llabre, M. M., Smith, S. R., Bizzotto, R., Santini, E., Manca, M. L., et al. (2015) · Diabetes · doi:10.2337/db15-0106 · Cited by 13
Self-citationThe Influence on Cardiovascular Mortality of the Metabolic Syndrome in Korean Postmenopausal Women
Shin, H. M., Jee, S. H., Kim, J. H., & Kim, M.-R. (2012) · Journal of Menopausal Medicine · doi:10.6118/jksm.2012.18.1.6 · Cited by 12
Balancing needs and means: the dilemma of the β‐cell in the modern world
Leibowitz, G., Kaiser, Ν., & Cerasi, E. (2009) · Diabetes Obesity and Metabolism · doi:10.1111/j.1463-1326.2009.01101.x · Cited by 12
Maguire, C. A., León, S., Carroll, R. S., Kaiser, U. B., & Navarro, V. M. (2017) · International Journal of Obesity · doi:10.1038/ijo.2017.185 · Cited by 12
“Metabolic characterization of Tac1 null mice under HFD (A and B) Percentage of lean (A) and fat (B) mass determined by MRI before (START) and after (END) four days of HFD (± SEM, n = 3/group).”
BackgroundInfluentialOrlando, A., Viazzi, F. C., Giussani, M., Nava, E., Cazzaniga, E., Bonino, B., Palestini, P., Parati, G., & Genovesi, S. (2019) · Hypertension Research · doi:10.1038/s41440-019-0253-3 · Cited by 12
Protective effect of DRB1 locus against type 2 diabetes mellitus in Mexican Mestizos
Pérez-Luque, E. L., Alaez, C., Malacara, J. M., Garay‐Sevilla, M. E., Fajardo, M. E., Nava, L. E., & Gorodezky, C. (2002) · Human Immunology · doi:10.1016/s0198-8859(02)00704-8 · Cited by 11
Prevalence of Metabolically Discordant Phenotypes in a Mediterranean Population—the Imap Study
Gómez-Huelgas, R., Narankiewicz, D., Villalobos, A., Wärnberǵ, J., Mancera‐Romero, J., Cuesta, A. L., Tinahones, F. J., & Bernal-López, M. R. (2013) · Endocrine Practice · doi:10.4158/ep12355.or · Cited by 12
Widdup, G., Bryson, J. R., Pawlak, D., Phuyal, J. L., Denyer, G. S., & Caterson, I. (2000) · European Journal of Endocrinology · doi:10.1530/eje.0.1430431 · Cited by 12
Extrapulmonary manifestations of pulmonary arterial hypertension
Singh, N., Al‐Naamani, N., Brown, M. B., Long, G., Thenappan, T., Umar, S., Ventetuolo, C. E., & Lahm, T. (2024) · Expert Review of Respiratory Medicine · doi:10.1080/17476348.2024.2361037 · Cited by 10
Insulin resistance is not necessarily an essential element of metabolic syndrome
Karnchanasorn, R., Ou, H.-Y., Chuang, L., & Chiu, K. C. (2012) · Endocrine · doi:10.1007/s12020-012-9702-3 · Cited by 12
Slavin, B. G., Zarow, C., Warden, C. H., & Fisler, J. S. (2009) · The Anatomical Record · doi:10.1002/ar.21019 · Cited by 11
“Insulin hypersecretion and insulin resistance has also been reported in human obesity (Ferrannini et al., 1997; Camastra et al., 2005).”
BackgroundSuccurro, E., Marini, M. A., Riccio, A., Fiorentino, T. V., Perticone, M., Sciacqua, A., Andreozzi, F., & Sesti, G. (2022) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2022.110185 · Cited by 11
Conséquences rénales de l’obésité
Laville, M. (2011) · Néphrologie & Thérapeutique · doi:10.1016/j.nephro.2010.11.007 · Cited by 11
Ybarra, J., Pou, J. M., Planas, F., Ballesta‐López, C., Echevarne, F., Romeo, J. H., & Navarro‐López, F. (2007) · Endocrine Practice · doi:10.4158/ep.13.6.590 · Cited by 11
Choi, M.-K., Han, Y.-A., & Roh, Y. K. (2014) · BMC Public Health · doi:10.1186/1471-2458-14-1166 · Cited by 11
“In several previous studies, MHO incidence has been assessed based on subsets of the 5 criteria for diagnosing metabolic syndrome, as we have done here [6,17-20].”
MethodAdipokine Pattern After Bariatric Surgery: Beyond the Weight Loss
Adami, G. F., Scopinaro, N., & Cordera, R. (2016) · Obesity Surgery · doi:10.1007/s11695-016-2347-1 · Cited by 12
“In physiological conditions, harmonic adipokine modifications follow the increase of the adipose tissue size: In humans, approximately 20 % of the obese population remains fully insulin-sensitive and metabolically normal, the metabolically health obese subject [78, 79].”
BackgroundLiu, A. W., Song, S. O., Hayashi, T., Satō, K., Kahn, S. E., Leonetti, D. L., Fujimoto, W. Y., & Boyko, E. J. (2019) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2019.06.008 · Cited by 11
“Although insulin resistance is seen more commonly in obesity, it also occurs in normal weight or overweight, and does not always accompany obesity [8,9].”
BackgroundTownsend, M. K., Okereke, O. I., Xia, W., Yang, T., Selkoe, D. J., & Grodstein, F. (2011) · Alzheimer Disease & Associated Disorders · doi:10.1097/wad.0b013e31821764ce · Cited by 11
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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