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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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Association of Increased Body Mass Index and Impaired Endothelial Function Among Hispanic Women
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Endothelium, Inflammation, and Diabetes
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“The suppressive effect of NO on PAI-1 may be diminished in certain pathophysiological states, such as obesity, insulin resistance, and type 2 diabetes, which display both reduced endothelium-dependent vasodilation 97,98 and elevated PAI-1 levels.”
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BackgroundThe Cardiometabolic Syndrome and Cardiovascular Disease
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BackgroundResultDeciphering Endothelial Dysfunction in the HIV-Infected Population
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“, 2000) and endothelial function (Steinberg et al., 1996) might be involved.”
BackgroundFree fatty acids/triglycerides increase ocular and subcutaneous blood flow
Polak, K., Schmetterer, L. F., Luksch, A., Gruber, S., Polska, E., Petternel, V., Bayerle‐Eder, M., Wolzt, M., Krebs, M., & Roden, M. (2001) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.2001.280.1.r56 · Cited by 20
“It is of note that in insulin-resistant subjects, the impairment of endothelium-dependent vascular reactivity is similar to the effect of a combined infusion of triglycerides and heparin in lean healthy volunteers (29, 30).”
ResultRegulation of Muscle Glucose Uptake In Vivo
Mandarino, L. J., Bonadonna, R. C., McGuinness, O. P., Halseth, A. E., & Wasserman, D. H. (2001) · Comprehensive physiology · doi:10.1002/cphy.cp070227 · Cited by 19
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Mertens, I. L., van der Planken, M., Corthouts, B., & Gaal, L. F. V. (2006) · Metabolism · doi:10.1016/j.metabol.2006.01.001 · Cited by 19
“Different studies have shown disturbances in endothelial-dependent vasodilatation in obese subjects [8,9], which seem to be closely related to an abdominal fat distribution as measured by the waist-tohip ratio (WHR) [9,10], waist circumference [9], or the amount of visceral adipose tissue (VAT) [11].”
BackgroundRoles of Renal Proximal Tubule Transport in Acid/Base Balance and Blood Pressure Regulation
Nakamura, M., Shirai, A., Yamazaki, O., Satoh, N., Suzuki, M., Horita, S., Yamada, H., & Seki, G. (2014) · BioMed Research International · doi:10.1155/2014/504808 · Cited by 19
“Notably, however, the vasodilator action of insulin is reported to be attenuated in insulin resistance [41, 42].”
BackgroundMansouri, M., Heshmat, R., Tabatabaei‐Malazy, O., Sharifi, F., Badamchizadeh, Z., Alatab, S., Omidfar, K., Fakhrzadeh, H., & Larijani, B. A. (2012) · Journal of Diabetes & Metabolic Disorders · doi:10.1186/2251-6581-11-2 · Cited by 18
Obesity alters the ovarian glucidic homeostasis disrupting the reproductive outcome of female rats
Bazzano, M. V., Paz, D. A., & Elia, E. M. (2017) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2017.01.003 · Cited by 19
Prevention of Cardiovascular Complications of Diabetes Mellitus by Aspirin
Nobles‐James, C., James, E. A., & Sowers, J. R. (2004) · Cardiovascular Drug Reviews · doi:10.1111/j.1527-3466.2004.tb00142.x · Cited by 19
Reboussin, D. M., Goff, D. C., Lipkin, E. W., Herrington, D. M., Summerson, J. H., Steffes, M. W., Crouse, R. J., Jovanovic, L. G., Feinglos, M. N., Probstfield, J. L., et al. (2004) · Diabetic Medicine · doi:10.1111/j.1464-5491.2004.01289.x · Cited by 18
Vicens Martí, C., Romeo, I., Aymat, R. M., García‐Picart, J., Val, P. G., Ballester, M., Aminian, N., Caralps, J. M., & Auge, J. M. (2001) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1067/mtc.2001.117836 · Cited by 19
Insights into the emerging cardiometabolic prevention and management of diabetes mellitus
Lastra‐González, G., Manrique, C. M., Govindarajan, G., Whaley‐Connell, A. T., & Sowers, J. R. (2005) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.6.13.2209 · Cited by 19
“Endothelial dysfunction can also be found in first-degree relatives of patients with DM2 [26], and in ageing and obese individuals [27], which confirms that insulin resistance, even without clinical diagnosis of DM2, is characterised by the impairment of the normal functions of the endothelium.”
BackgroundInsulin Resistance and Endothelial Dysfunction in Atherosclerosis: Implications and Interventions
Dandona, P. (2002) · Diabetes Technology & Therapeutics · doi:10.1089/152091502321118829 · Cited by 19
“16,17 In patients with type 2 diabetes, insulin resistance and endothelial dysfunction both precede the development of overt hyperglycemia.”
Acetylcarnitine Is Associated With Cardiovascular Disease Risk in Type 2 Diabetes Mellitus
Zhao, S., Liu, M.-L., Huang, B., Zhao, F., Li, Y., Cui, X.-T., & Lin, R. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.806819 · Cited by 18
“Insulin resistance is associated with reduced production and release of nitric oxide in vascular endothelial cells (38), leading to impaired cellular function and, thus, an increased risk of atherosclerosis (39).”
BackgroundObesity, Preserved Ejection Fraction Heart Failure, and Left Ventricular Remodeling
Stencel, J. D., Alai, H. R., Dhore-Patil, A., Urina‐Jassir, D., & Jemtel, T. H. L. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12093341 · Cited by 20
Microvascular Skeletal-Muscle Crosstalk in Health and Disease
Pepe, G. J., & Albrecht, E. D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241310425 · Cited by 19
Vyssoulis, G. P., Pietri, P., Vlachopoulos, C. V., Alexopoulos, N. A., Kyvelou, S.-M., Terentes-Printzios, D. G., & Stefanadis, C. (2011) · Diabetes and Vascular Disease Research · doi:10.1177/1479164111422827 · Cited by 18
Tangvarasittichai, S., Pongthaisong, S., Meemark, S., & Tangvarasittichai, O. (2014) · Indian Journal of Clinical Biochemistry · doi:10.1007/s12291-014-0443-3 · Cited by 18
Endothelial dysfunction in myometrial arteries of women with gestational diabetes
Chirayath, H. H., Wareing, M., Taggart, M. J., & Baker, P. N. (2010) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2010.03.022 · Cited by 18
The role of vascular failure in coronary artery spasm
Kawano, H., & Node, K. (2010) · Journal of Cardiology · doi:10.1016/j.jjcc.2010.08.007 · Cited by 18
John, C. M., Khaddaj‐Mallat, R., George, G., Kim, T., Mishra, R. C., & Braun, A. P. (2018) · Channels · doi:10.1080/19336950.2018.1454814 · Cited by 22
“In further support, studies have shown that endothelium-dependent vasodilation is reduced by 40–50% in obese patients when compared with lean patients [66].”
BackgroundSathya Bhama, C. V. (2012) · JOURNAL OF CLINICAL AND DIAGNOSTIC RESEARCH · doi:10.7860/jcdr/2012/4377.2646 · Cited by 18
“Moreover, the individuals who are relatively insensitive to the insulin-mediated glucose uptake also appear to have a corresponding decrease in the basal endothelial nitric oxide production [19].”
Backgroundden Hertog, H. M., Vermeer, S. E., Zandbergen, A. A. M., Achterberg, S., Dippel, D. W. J., Algra, A., Kappelle, L. J., & Koudstaal, P. J. (2013) · International Journal of Stroke · doi:10.1111/ijs.12023 · Cited by 18
Hypopituitarism and atherosclerosis
Elbadd, T. A., Abdu, T. A. M., & Clayton, R. N. (2001) · Annals of Medicine · doi:10.3109/07853890109002097 · Cited by 18
Stimulatory Effect of Leptin on Nitric Oxide Production Is Impaired in Dietary‐Induced Obesity
Bełtowski, J., Wójcicka, G., & Jamroz, A. (2003) · Obesity Research · doi:10.1038/oby.2003.209 · Cited by 18
Acute effects of elevated NEFA on vascular function: a comparison of SFA and MUFA
Newens, K. J., Thompson, A. K., Jackson, K. G., Wright, J., & Williams, C. M. (2010) · British Journal Of Nutrition · doi:10.1017/s0007114510004976 · Cited by 19
“Experimental elevation of plasma NEFA using intravenous infusion of lipid and heparin also results in impaired insulin-stimulated glucose uptake in skeletal muscle((3)) and endothelial dysfunction((4)), both of which are key features of T2D and obesity((5,6)).”
Nangle, M. R., Proietto, J., & Keast, J. R. (2009) · The Journal of Sexual Medicine · doi:10.1111/j.1743-6109.2009.01415.x · Cited by 17
Aortic function is compromised in a rat model of polycystic ovary syndrome
Lakhani, K., Yang, W., Dooley, A., El-Mahdi, E., Sundaresan, M., McLellan, S., Bruckdorfer, R. K., Leonard, A., Seifalian, A. M., & Hardiman, P. J. (2005) · Human Reproduction · doi:10.1093/humrep/dei399 · Cited by 18
“The elevated serum testosterone in mifepristone-treated rats could diminish vasodilatory responses to ACh, since in PCOS women, leg blood flow response to methacholine is negatively correlated with serum testosterone (Steinberg et al., 1996; Paradisi et al., 2003).”
BackgroundA clinical comparative study of the management of chronic renal failure with Punarnavadi compound
Prashanth, G., Baghel, M., Ravishankar, B., Sn, G., & Mehta, M. (2010) · AYU (An International Quarterly Journal of Research in Ayurveda) · doi:10.4103/0974-8520.72388 · Cited by 18
“Diabetes and hypertension are the important causes for renal failure and their incidence is raising world wide.[3-6] Irrespective of the underlying mechanisms, elevated levels of blood glucose ignite a vicious cycle of metabolic disturbances within the intracellular and extracellular environment that, if left unchecke…”
BackgroundRauchfuss, S., Geiger, J., Walter, U., Renné, T., & Gambaryan, S. P. (2008) · Journal of Thrombosis and Haemostasis · doi:10.1111/j.1538-7836.2008.02925.x · Cited by 18
Migdalis, I. N., Kalogeropoulou, K., ILIOPOULOU, V., Triantafilou, P., Charalabides, J., MORTZOS, G., & Cordopatis, C. (2001) · Diabetes Research and Clinical Practice · doi:10.1016/s0168-8227(01)00275-3 · Cited by 18
“Prostacyclin was recognized to be an endothelium-derived relaxing substance [6,7].”
BackgroundAlterations in nitric oxide-cGMP pathway in ventricular myocytes from obese leptin-deficient mice
Su, J., Zhang, S., Tse, J., Scholz, P. M., & Weiss, H. R. (2003) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00316.2003 · Cited by 12
“Our results were consistent with a previous clinical study where an exogenous NO donor produced similar negative hemodynamic responses between obese and lean subjects (26).”
ResultVilla, E., Rabano, A., Albarran, O. G., Ruilope, L. M., & Garcia-Robles, R. (1998) · American Journal of Hypertension · doi:10.1016/s0895-7061(98)00053-3 · Cited by 11
“Although some controversy still remains about the intimate mechanism responsible for this metabolic derangement, it has recently been pointed out that the endothelium of the skeletal muscle vasculature is the main target for the deleterious actions leading to impaired insulin-mediated vasodilation in obese humans.(1)…”
MethodMoore, M. N., Climie, R. E., Otahal, P., & Schultz, M. G. (2021) · Journal of Hypertension · doi:10.1097/hjh.0000000000002962 · Cited by 23
“A poorer metabolic and lipid profile may contribute towards functional and structural decline of the microvasculature [37,38].”
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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