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Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance
Open accessAbstract
To test the hypothesis that obesity/insulin resistance impairs both endothelium-dependent vasodilation and insulin-mediated augmentation of endothelium-dependent vasodilation, we studied leg blood flow (LBF) responses to graded intrafemoral artery infusions of methacholine chloride (MCh) or sodium nitroprusside (SNP) during saline infusion and euglycemic hyperinsulinemia in lean insulin-sensitive controls (C), in obese insulin-resistant subjects (OB), and in subjects with non-insulin-dependent diabetes mellitus (NIDDM). MCh induced increments in LBF were approximately 40% and 55% lower in OB and NIDDM, respectively, as compared with C (P < 0.05). Euglycemic hyperinsulinemia augmented the LBF response to MCh by - 50% in C (P < 0.05 vs saline) but not in OB and NIDDM. SNP caused comparable increments in LBF in all groups. Regression analysis revealed a significant inverse correlation between the maximal LBF change in response to MCh and body fat content. Thus, obesity/insulin resistance is associated with (a) blunted endothelium-dependent, but normal endothelium-independent vasodilation and (b) failure of euglycemic hyperinsulinemia to augment endothelium-dependent vasodilation. Therefore, obese/insulin-resistant subjects are characterized by endothelial dysfunction and endothelial resistance to insulin's effect on enhancement of endothelium-dependent vasodilation. This endothelial dysfunction could contribute to the increased risk of atherosclerosis in obese insulin-resistant subjects.
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“Furthermore, IR per se has a direct impact on endothelial function, distinct from effects related to unfavorable changes in lipid composition or blood pressure (9).”
From Improved Endothelial Function With Metformin in Type 2 Diabetes Mellitus (2001) · cites this paper as [9]
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Aziz, A., & Wheatcroft, S. B. (2011) · Expert Review of Cardiovascular Therapy · doi:10.1586/erc.11.20 · Cited by 25
Musa, M. G., Torrens, C., & Clough, G. F. (2013) · Acta Physiologica · doi:10.1111/apha.12131 · Cited by 25
“…dilation has been reported in numerous human studies in cardiometabolic disease both in larger arteries using flowmediated dilatation (FMD) and within the microvasculature using non-invasive imaging of the skin and deeper tissues (Steinberg et al. 1996, de Jongh et al. 2008, Kabutoya et al. 2012).”
Metabolic disturbances linked to obesity: the role of impaired tissue perfusion
Villela, N. R., Kraemer‐Aguiar, L. G., Bottino, D. A., Wiernsperger, N. F., & Bouskela, E. (2009) · Arquivos Brasileiros de Endocrinologia & Metabologia · doi:10.1590/s0004-27302009000200015 · Cited by 25
Kraemer‐Aguiar, L. G., Maranhao, P. A., Cyrino, F. Z. G. A., & Bouskela, E. (2010) · Microvascular Research · doi:10.1016/j.mvr.2010.08.004 · Cited by 25
Bressler, J., Pankow, J. S., Coresh, J., & Boerwinkle, E. (2013) · PLoS ONE · doi:10.1371/journal.pone.0079466 · Cited by 25
“[32,45,51,52] Insulin has direct effects on the vasculature by stimulating the production of NO in endothelial cells through the P13-kinase/Akt pathway [53–57].”
BackgroundPasimeni, G., Ribaudo, M. C., Capoccia, D., Rossi, F., Bertone, C., Leonetti, F., & Santiemma, V. (2006) · Microvascular Research · doi:10.1016/j.mvr.2005.12.001 · Cited by 27
Freidja, M. L., Vessières, E., Toutain, B., Guihot, A., Custaud, M., Loufrani, L., Fassot, C., & Henrion, D. (2014) · Cardiovascular Diabetology · doi:10.1186/1475-2840-13-55 · Cited by 25
“ALT-711 did not improve flow-mediated remodeling in one-year old ZDF rats Type 2 diabetes reduced the capacity of the endothelium to induce vasodilatation, especially in resistance arteries [31].”
BackgroundCalf flow reserve with H(2)(15)O PET as a quantifiable index of lower extremity flow.
Schmidt, M. A., Chakrabarti, A., Shamim-Uzzaman, Q. A., Kaciroti, N., Koeppe, R. A., & Rajagopalan, S. (2003) · PubMed · Cited by 25
Antiobesogenic Role of Endothelial Nitric Oxide Synthase
Sansbury, B. E., & Hill, B. G. (2014) · Vitamins and hormones · doi:10.1016/b978-0-12-800254-4.00013-1 · Cited by 26
Soares, A. G., de Carvalho, M. H. C., & Akamine, E. H. (2017) · BioMed Research International · doi:10.1155/2017/5038602 · Cited by 25
Černý, D., Sartori, C. S., Rimoldi, S. F., Meister, T. A., Soria, R., Bouillet, E., Scherrer, U., & Rexhaj, E. (2017) · Endocrinology · doi:10.1210/en.2016-1475 · Cited by 25
Madkhali, H. A. (2020) · Saudi Pharmaceutical Journal · doi:10.1016/j.jsps.2020.01.009 · Cited by 25
“Several human and experimental studies have linked ED to obesity and obesity-associated cardio-vascular diseases (Steinberg et al., 1996; Vita et al., 2002).”
Qin, B., Nagasaki, M., Ren, M., Bajotto, G., Oshida, Y., & Sato, Y. (2003) · Life Sciences · doi:10.1016/s0024-3205(03)00640-4 · Cited by 25
Hypertension and insulin disorders
Imazu, M. (2002) · Current Hypertension Reports · doi:10.1007/s11906-002-0029-y · Cited by 25
“Insulin resistance states such as hypertension are associated with impaired endotheliumdependent vasodilatation [ 32 ].”
BackgroundLovegrove, J. A. (2007) · Proceedings of The Nutrition Society · doi:10.1017/s0029665107005514 · Cited by 25
“(Patsch et al. 1992; Steinberg et al. 1996; Alberti & Zimmet, 1998; Austin et al. 1998).”
BackgroundSayin, E., Sayın, B., Ertuğrul, İbis, Sezer, S., & Özdemir, Ö. (2013) · International Journal of Nephrology and Renovascular Disease · doi:10.2147/ijnrd.s41384 · Cited by 24
Sanchez, O. A., Copenhaver, E. A., Chance, M. A., Fowler, M. J., Towse, T. F., Kent‐Braun, J. A., & Damon, B. M. (2011) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00060.2011 · Cited by 25
Atherothrombotic risk in obesity
Vera, R. H., Vilahur, G., & Badimón, L. (2013) · Hämostaseologie · doi:10.5482/hamo-13-07-0034 · Cited by 24
Badhwar, S., Chandran, D. S., Jaryal, A. K., Narang, R., & Deepak, K. K. (2017) · Diabetes and Vascular Disease Research · doi:10.1177/1479164117748840 · Cited by 25
Vizzardi, E., Gavazzoni, M., Pina, P. D., Bonadei, I., Regazzoni, V., Sciatti, E., Trichaki, E., Raddino, R., & Metra, M. (2014) · Journal of Investigative Medicine · doi:10.1097/jim.0000000000000096 · Cited by 24
Hamer, M., & Boutcher, S. (2006) · Journal of Human Hypertension · doi:10.1038/sj.jhh.1002035 · Cited by 18
Keller, J., Mandalà, M., Casson, P. R., & Osol, G. (2011) · Endocrinology · doi:10.1210/en.2011-1424 · Cited by 24
“Although the association between insulin resistance and endothelial dysfunction has been clearly demonstrated in young obese subjects without PCOS (14), clinical research in PCOS patients suggests an association with endothelial dysfunction that is greater than that accounted for by insulin resistance alone (15–17).”
BackgroundPrior Exercise and Postprandial Incretin Responses in Lean and Obese Individuals
Heden, T. D., Liu, Y., Kearney, M. L., Park, Y., Dellsperger, K. C., Thomas, T. R., & Kanaley, J. A. (2013) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318294b225 · Cited by 24
“A bnormally elevated postprandial triacylglycerol (TAG) (21) and insulin (16) concentrations increase the risk of cardiovascular disease as both are associated with endothelial dysfunction (23,33), an early event in the atherosclerotic process.”
BackgroundWang, X., Lockhart, S. M., Rathjen, T., Albadawi, H., Sørensen, D., O'Neill, B. T., Dwivedi, N., Preil, S. R., Beck, H. C., Dunwoodie, S. L., et al. (2016) · Diabetes · doi:10.2337/db16-0001 · Cited by 24
“Consistent with this mechanism, the bioavailability of endothelial-derived NO is decreased in patients with diabetes (13,14).”
BackgroundResultRaji, A., Gerhard‐Herman, M. D., Williams, J. S., O’Connor, M. E., & Simonson, D. C. (2006) · Diabetic Medicine · doi:10.1111/j.1464-5491.2006.01843.x · Cited by 24
Ohashi, N., Ito, C., Fujikawa, R., Yamamoto, H., Kihara, Y., & Kohno, N. (2009) · Metabolism · doi:10.1016/j.metabol.2009.03.005 · Cited by 24
“reported to be associated with decreased endothelium-dependent vasodilation [23] and increased arterial stiffness [24].”
Background
Metadata
- Authors
- Steinberg, H. O., Chaker, H., Leaming, R., Johnson, A., Brechtel, G., & Baron, A. D.
- Affiliations
- Indiana University (US)
- Richard L. Roudebush VA Medical Center (US)
- Indiana University Hospital (US)
- Venue
- Journal of Clinical Investigation
- Published
- 1996-06-01
- Volume
- 97
- Issue
- 11
- Pages
- 2601-2610
- ISSN
- 0021-9738 (ISSN-L)
- PMC
- PMC507347
- OpenAlex
- W1982811953
- Cited by
- 1,687
- References
- 59
- Citations by year
- 2026: 11 · 2025: 23 · 2024: 17 · 2023: 30 · 2022: 19 · 2021: 32 · 2020: 30 · 2019: 36 · 2018: 36 · 2017: 46 · 2016: 50 · 2015: 51 · 2014: 69 · 2013: 69 · 2012: 61
- FWCI
- 18.69
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Clinical Investigation (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Veterans Affairs
- American Heart Association
- National Institutes of Health
- National Institute of Diabetes and Digestive and Kidney Diseases (DK42469, P60DK020542, DK20542)
- National Center for Research Resources (M 01-RR750-19)
- Topics
- Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Health and Disease Prevention
- Keywords
- obesity, insulin resistance, endothelial dysfunction, endothelium-dependent vasodilation, euglycemic hyperinsulinemia, leg blood flow, methacholine, sodium nitroprusside, type 2 diabetes, fat mass, atherosclerosis risk
- MeSH terms
- Adult, Blood Glucose, Blood Pressure, Cholesterol, Diabetes Mellitus, Type 2, Endothelium, Vascular, Fatty Acids, Nonesterified, Glucose, Humans, Hyperinsulinism, Infusions, Intra-Arterial, Infusions, Intravenous, Insulin, Insulin Resistance, Leg, Cholesterol, HDL, Cholesterol, LDL, Nitroprusside, Obesity, Reference Values, Regional Blood Flow, Syndrome, Time Factors, Triglycerides, Vasodilation, Glucose Clamp Technique, Body Mass Index, Methacholine Chloride
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