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Published in: Cardiovascular Diabetology 1/2019

Open Access 01-12-2019 | Insulins | Original investigation

Temporal relationship between inflammation and insulin resistance and their joint effect on hyperglycemia: the Bogalusa Heart Study

Authors: Yinkun Yan, Shengxu Li, Yang Liu, Lydia Bazzano, Jiang He, Jie Mi, Wei Chen

Published in: Cardiovascular Diabetology | Issue 1/2019

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Abstract

Background

Inflammation and insulin resistance play crucial roles in the development of type 2 diabetes mellitus (T2DM). We aim to examine the temporal relationship between high-sensitivity C-reactive protein (hsCRP) and insulin resistance in non-diabetic adults and their joint effect on the development of hyperglycemia.

Methods

The longitudinal cohort from the Bogalusa Heart Study consisted of 509 non-diabetic adults (360 whites and 149 blacks, mean age = 42.8 years at follow-up) who had hsCRP, fasting glucose and insulin measured twice at baseline and follow-up over 6.8 years. Cross-lagged panel model was used to examine the temporal relationship between hsCRP and homeostasis model assessment for insulin resistance (HOMA-IR). Information on incident T2DM was collected in a survey in 6.1 years after the follow-up survey.

Results

After adjusting for race, sex, age, body mass index, smoking, alcohol drinking and follow-up years, the path coefficient from baseline hsCRP to follow-up HOMA-IR (β2 = 0.105, p = 0.009) was significant and greater than the path from baseline HOMA-IR to follow-up hsCRP (β1 = 0.005, p = 0.903), with p = 0.011 for the difference between β1 and β2. This one-directional path from baseline hsCRP to follow-up HOMA-IR was significant in the hyperglycemia group but not in the normoglycemia group. In addition, participants with high levels of baseline hsCRP and follow-up HOMA-IR had greater risks of T2DM (odds ratio, OR = 2.38, p = 0.035), pre-T2DM (OR = 2.27, p = 0.006) and hyperglycemia (OR = 2.18, p = 0.003) than those with low–low levels.

Conclusions

These findings suggest that elevated hsCRP is associated with future insulin resistance in non-diabetic adults, and their joint effect is predictive of the development of T2DM.
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Literature
1.
go back to reference Duncan BB, Schmidt MI, Pankow JS, Ballantyne CM, Couper D, Vigo A, Hoogeveen R, Folsom AR, Heiss G. Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes. 2003;52(7):1799–805.PubMedCrossRef Duncan BB, Schmidt MI, Pankow JS, Ballantyne CM, Couper D, Vigo A, Hoogeveen R, Folsom AR, Heiss G. Low-grade systemic inflammation and the development of type 2 diabetes: the atherosclerosis risk in communities study. Diabetes. 2003;52(7):1799–805.PubMedCrossRef
2.
go back to reference Donath MY. Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov. 2014;13(6):465–76.PubMedCrossRef Donath MY. Targeting inflammation in the treatment of type 2 diabetes: time to start. Nat Rev Drug Discov. 2014;13(6):465–76.PubMedCrossRef
3.
go back to reference Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11(2):98–107.PubMedCrossRef Donath MY, Shoelson SE. Type 2 diabetes as an inflammatory disease. Nat Rev Immunol. 2011;11(2):98–107.PubMedCrossRef
4.
go back to reference Ebtehaj S, Gruppen EG, Parvizi M, Tietge U, Dullaart R. The anti-inflammatory function of HDL is impaired in type 2 diabetes: role of hyperglycemia, paraoxonase-1 and low grade inflammation. Cardiovasc Diabetol. 2017;16(1):132.PubMedPubMedCentralCrossRef Ebtehaj S, Gruppen EG, Parvizi M, Tietge U, Dullaart R. The anti-inflammatory function of HDL is impaired in type 2 diabetes: role of hyperglycemia, paraoxonase-1 and low grade inflammation. Cardiovasc Diabetol. 2017;16(1):132.PubMedPubMedCentralCrossRef
5.
go back to reference Kaptoge S, Di Angelantonio E, Lowe G, Pepys MB, Thompson SG, Collins R, Danesh J. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet. 2010;375(9709):132–40.PubMedCrossRef Kaptoge S, Di Angelantonio E, Lowe G, Pepys MB, Thompson SG, Collins R, Danesh J. C-reactive protein concentration and risk of coronary heart disease, stroke, and mortality: an individual participant meta-analysis. Lancet. 2010;375(9709):132–40.PubMedCrossRef
6.
go back to reference Bao X, Borne Y, Johnson L, Muhammad IF, Persson M, Niu K, Engstrom G. Comparing the inflammatory profiles for incidence of diabetes mellitus and cardiovascular diseases: a prospective study exploring the ‘common soil’ hypothesis. Cardiovasc Diabetol. 2018;17(1):87.PubMedPubMedCentralCrossRef Bao X, Borne Y, Johnson L, Muhammad IF, Persson M, Niu K, Engstrom G. Comparing the inflammatory profiles for incidence of diabetes mellitus and cardiovascular diseases: a prospective study exploring the ‘common soil’ hypothesis. Cardiovasc Diabetol. 2018;17(1):87.PubMedPubMedCentralCrossRef
7.
go back to reference Ridker PM, MacFadyen JG, Everett BM, Libby P, Thuren T, Glynn RJ. Relationship of C-reactive protein reduction to cardiovascular event reduction following treatment with canakinumab: a secondary analysis from the CANTOS randomised controlled trial. Lancet. 2018;391(10118):319–28.PubMedCrossRef Ridker PM, MacFadyen JG, Everett BM, Libby P, Thuren T, Glynn RJ. Relationship of C-reactive protein reduction to cardiovascular event reduction following treatment with canakinumab: a secondary analysis from the CANTOS randomised controlled trial. Lancet. 2018;391(10118):319–28.PubMedCrossRef
8.
go back to reference Yang W, Li Y, Wang JY, Han R, Wang L. Circulating levels of adipose tissue-derived inflammatory factors in elderly diabetes patients with carotid atherosclerosis: a retrospective study. Cardiovasc Diabetol. 2018;17(1):75.PubMedPubMedCentralCrossRef Yang W, Li Y, Wang JY, Han R, Wang L. Circulating levels of adipose tissue-derived inflammatory factors in elderly diabetes patients with carotid atherosclerosis: a retrospective study. Cardiovasc Diabetol. 2018;17(1):75.PubMedPubMedCentralCrossRef
9.
go back to reference Herder C, Kannenberg JM, Carstensen-Kirberg M, Huth C, Meisinger C, Koenig W, Peters A, Rathmann W, Roden M, Thorand B. Serum levels of interleukin-22, cardiometabolic risk factors and incident type 2 diabetes: KORA F4/FF4 study. Cardiovasc Diabetol. 2017;16(1):17.PubMedPubMedCentralCrossRef Herder C, Kannenberg JM, Carstensen-Kirberg M, Huth C, Meisinger C, Koenig W, Peters A, Rathmann W, Roden M, Thorand B. Serum levels of interleukin-22, cardiometabolic risk factors and incident type 2 diabetes: KORA F4/FF4 study. Cardiovasc Diabetol. 2017;16(1):17.PubMedPubMedCentralCrossRef
10.
go back to reference Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286(3):327–34.PubMedCrossRef Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. JAMA. 2001;286(3):327–34.PubMedCrossRef
11.
go back to reference Wang X, Bao W, Liu J, Ouyang YY, Wang D, Rong S, Xiao X, Shan ZL, Zhang Y, Yao P, et al. Inflammatory markers and risk of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care. 2013;36(1):166–75.PubMedCrossRef Wang X, Bao W, Liu J, Ouyang YY, Wang D, Rong S, Xiao X, Shan ZL, Zhang Y, Yao P, et al. Inflammatory markers and risk of type 2 diabetes: a systematic review and meta-analysis. Diabetes Care. 2013;36(1):166–75.PubMedCrossRef
12.
go back to reference Festa A, D’Agostino R, Howard G, Mykkänen L, Tracy RP, Haffner SM. Chronic subclinical inflammation as part of the insulin resistance syndrome: the Insulin Resistance Atherosclerosis Study (IRAS). Circulation. 2000;102(1):42–7.PubMedCrossRef Festa A, D’Agostino R, Howard G, Mykkänen L, Tracy RP, Haffner SM. Chronic subclinical inflammation as part of the insulin resistance syndrome: the Insulin Resistance Atherosclerosis Study (IRAS). Circulation. 2000;102(1):42–7.PubMedCrossRef
13.
go back to reference Wu T, Dorn JP, Donahue RP, Sempos CT, Trevisan M. Associations of serum C-reactive protein with fasting insulin, glucose, and glycosylated hemoglobin: the Third National Health and Nutrition Examination Survey, 1988–1994. Am J Epidemiol. 2002;155(1):65–71.PubMedCrossRef Wu T, Dorn JP, Donahue RP, Sempos CT, Trevisan M. Associations of serum C-reactive protein with fasting insulin, glucose, and glycosylated hemoglobin: the Third National Health and Nutrition Examination Survey, 1988–1994. Am J Epidemiol. 2002;155(1):65–71.PubMedCrossRef
14.
go back to reference Kahn SE, Zinman B, Haffner SM, O’Neill MC, Kravitz BG, Yu D, Freed MI, Herman WH, Holman RR, Jones NP, et al. Obesity is a major determinant of the association of C-reactive protein levels and the metabolic syndrome in type 2 diabetes. Diabetes. 2006;55(8):2357–64.PubMedCrossRef Kahn SE, Zinman B, Haffner SM, O’Neill MC, Kravitz BG, Yu D, Freed MI, Herman WH, Holman RR, Jones NP, et al. Obesity is a major determinant of the association of C-reactive protein levels and the metabolic syndrome in type 2 diabetes. Diabetes. 2006;55(8):2357–64.PubMedCrossRef
15.
go back to reference Chen L, Chen R, Wang H, Liang F. Mechanisms linking inflammation to insulin resistance. Int J Endocrinol. 2015;2015:508409.PubMedPubMedCentral Chen L, Chen R, Wang H, Liang F. Mechanisms linking inflammation to insulin resistance. Int J Endocrinol. 2015;2015:508409.PubMedPubMedCentral
16.
go back to reference Shimobayashi M, Albert V, Woelnerhanssen B, Frei IC, Weissenberger D, Meyer-Gerspach AC, Clement N, Moes S, Colombi M, Meier JA, et al. Insulin resistance causes inflammation in adipose tissue. J Clin Invest. 2018;128(4):1538–50.PubMedPubMedCentralCrossRef Shimobayashi M, Albert V, Woelnerhanssen B, Frei IC, Weissenberger D, Meyer-Gerspach AC, Clement N, Moes S, Colombi M, Meier JA, et al. Insulin resistance causes inflammation in adipose tissue. J Clin Invest. 2018;128(4):1538–50.PubMedPubMedCentralCrossRef
17.
go back to reference Savage DB, Petersen KF, Shulman GI. Mechanisms of insulin resistance in humans and possible links with inflammation. Hypertension. 2005;45(5):828–33.PubMedCrossRef Savage DB, Petersen KF, Shulman GI. Mechanisms of insulin resistance in humans and possible links with inflammation. Hypertension. 2005;45(5):828–33.PubMedCrossRef
18.
go back to reference Park K, Steffes M, Lee DH, Himes JH, Jacobs DR. Association of inflammation with worsening HOMA-insulin resistance. Diabetologia. 2009;52(11):2337–44.PubMedPubMedCentralCrossRef Park K, Steffes M, Lee DH, Himes JH, Jacobs DR. Association of inflammation with worsening HOMA-insulin resistance. Diabetologia. 2009;52(11):2337–44.PubMedPubMedCentralCrossRef
19.
go back to reference Herder C, Færch K, Carstensen-Kirberg M, Lowe GD, Haapakoski R, Witte DR, Brunner EJ, Roden M, Tabák AG, Kivimäki M, et al. Biomarkers of subclinical inflammation and increases in glycaemia, insulin resistance and beta-cell function in non-diabetic individuals: the Whitehall II study. Eur J Endocrinol. 2016;175(5):367–77.PubMedCrossRef Herder C, Færch K, Carstensen-Kirberg M, Lowe GD, Haapakoski R, Witte DR, Brunner EJ, Roden M, Tabák AG, Kivimäki M, et al. Biomarkers of subclinical inflammation and increases in glycaemia, insulin resistance and beta-cell function in non-diabetic individuals: the Whitehall II study. Eur J Endocrinol. 2016;175(5):367–77.PubMedCrossRef
20.
go back to reference Uemura H, Katsuura-Kamano S, Yamaguchi M, Bahari T, Ishizu M, Fujioka M, Arisawa K. Relationships of serum high-sensitivity C-reactive protein and body size with insulin resistance in a Japanese cohort. PLoS ONE. 2017;12(6):e0178672.PubMedPubMedCentralCrossRef Uemura H, Katsuura-Kamano S, Yamaguchi M, Bahari T, Ishizu M, Fujioka M, Arisawa K. Relationships of serum high-sensitivity C-reactive protein and body size with insulin resistance in a Japanese cohort. PLoS ONE. 2017;12(6):e0178672.PubMedPubMedCentralCrossRef
21.
go back to reference Gala T, Herder C, Rutters F, Carstensen-Kirberg M, Huth C, Stehouwer C, Nijpels G, Schalkwijk C, Flyvbjerg A, Franks PW, et al. Association of changes in inflammation with variation in glycaemia, insulin resistance and secretion based on the KORA study. Diabetes Metab Res Rev. 2018;34(8):e3063.CrossRef Gala T, Herder C, Rutters F, Carstensen-Kirberg M, Huth C, Stehouwer C, Nijpels G, Schalkwijk C, Flyvbjerg A, Franks PW, et al. Association of changes in inflammation with variation in glycaemia, insulin resistance and secretion based on the KORA study. Diabetes Metab Res Rev. 2018;34(8):e3063.CrossRef
22.
go back to reference Brunner EJ, Kivimäki M, Witte DR, Lawlor DA, Davey Smith G, Cooper JA, Miller M, Lowe GD, Rumley A, Casas JP, et al. Inflammation, insulin resistance, and diabetes–Mendelian randomization using CRP haplotypes points upstream. PLoS Med. 2008;5(8):e155.PubMedPubMedCentralCrossRef Brunner EJ, Kivimäki M, Witte DR, Lawlor DA, Davey Smith G, Cooper JA, Miller M, Lowe GD, Rumley A, Casas JP, et al. Inflammation, insulin resistance, and diabetes–Mendelian randomization using CRP haplotypes points upstream. PLoS Med. 2008;5(8):e155.PubMedPubMedCentralCrossRef
23.
go back to reference Noordam R, Oudt CH, Bos MM, Smit R, van Heemst D. High-sensitivity C-reactive protein, low-grade systemic inflammation and type 2 diabetes mellitus: a two-sample Mendelian randomization study. Nutr Metab Cardiovasc Dis. 2018;28(8):795–802.PubMedCrossRef Noordam R, Oudt CH, Bos MM, Smit R, van Heemst D. High-sensitivity C-reactive protein, low-grade systemic inflammation and type 2 diabetes mellitus: a two-sample Mendelian randomization study. Nutr Metab Cardiovasc Dis. 2018;28(8):795–802.PubMedCrossRef
24.
go back to reference Berenson GS. Bogalusa Heart Study: a long-term community study of a rural biracial (black/white) population. Am J Med Sci. 2001;322(5):267–74.PubMedCrossRef Berenson GS. Bogalusa Heart Study: a long-term community study of a rural biracial (black/white) population. Am J Med Sci. 2001;322(5):267–74.PubMedCrossRef
25.
go back to reference Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.PubMedCrossRef Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia. 1985;28(7):412–9.PubMedCrossRef
26.
go back to reference Kenny DA. Cross-lagged panel correlation: a test for spuriousness. Psychol Bull. 1975;82:887–903.CrossRef Kenny DA. Cross-lagged panel correlation: a test for spuriousness. Psychol Bull. 1975;82:887–903.CrossRef
27.
go back to reference Kivimäki M, Feldt T, Vahtera J, Nurmi JE. Sense of coherence and health: evidence from two cross-lagged longitudinal samples. Soc Sci Med. 2000;50(4):583–97.PubMedCrossRef Kivimäki M, Feldt T, Vahtera J, Nurmi JE. Sense of coherence and health: evidence from two cross-lagged longitudinal samples. Soc Sci Med. 2000;50(4):583–97.PubMedCrossRef
28.
go back to reference Joreskog K, Sorbom D. LISREL 8.52: User’s Reference Guide. 2001. Chicago. Scientifc Software International. Joreskog K, Sorbom D. LISREL 8.52: User’s Reference Guide. 2001. Chicago. Scientifc Software International.
29.
go back to reference Ormazabal V, Nair S, Elfeky O, Aguayo C, Salomon C, Zuniga FA. Association between insulin resistance and the development of cardiovascular disease. Cardiovasc Diabetol. 2018;17(1):122.PubMedPubMedCentralCrossRef Ormazabal V, Nair S, Elfeky O, Aguayo C, Salomon C, Zuniga FA. Association between insulin resistance and the development of cardiovascular disease. Cardiovasc Diabetol. 2018;17(1):122.PubMedPubMedCentralCrossRef
30.
go back to reference Van Gaal LF, Mertens IL, De Block CE. Mechanisms linking obesity with cardiovascular disease. Nature. 2006;444(7121):875–80.PubMedCrossRef Van Gaal LF, Mertens IL, De Block CE. Mechanisms linking obesity with cardiovascular disease. Nature. 2006;444(7121):875–80.PubMedCrossRef
31.
go back to reference Natali A, Toschi E, Baldeweg S, Ciociaro D, Favilla S, Saccà L, Ferrannini E. Clustering of insulin resistance with vascular dysfunction and low-grade inflammation in type 2 diabetes. Diabetes. 2006;55(4):1133–40.PubMedCrossRef Natali A, Toschi E, Baldeweg S, Ciociaro D, Favilla S, Saccà L, Ferrannini E. Clustering of insulin resistance with vascular dysfunction and low-grade inflammation in type 2 diabetes. Diabetes. 2006;55(4):1133–40.PubMedCrossRef
32.
go back to reference Meng YX, Ford ES, Li C, Quarshie A, Al-Mahmoud AM, Giles W, Gibbons GH, Strayhorn G. Association of C-reactive protein with surrogate measures of insulin resistance among nondiabetic US from National Health and Nutrition Examination Survey 1999–2002. Clin Chem. 2007;53(12):2152–9.PubMedCrossRef Meng YX, Ford ES, Li C, Quarshie A, Al-Mahmoud AM, Giles W, Gibbons GH, Strayhorn G. Association of C-reactive protein with surrogate measures of insulin resistance among nondiabetic US from National Health and Nutrition Examination Survey 1999–2002. Clin Chem. 2007;53(12):2152–9.PubMedCrossRef
33.
go back to reference Deepa R, Velmurugan K, Arvind K, Sivaram P, Sientay C, Uday S, Mohan V. Serum levels of interleukin 6, C-reactive protein, vascular cell adhesion molecule 1, and monocyte chemotactic protein 1 in relation to insulin resistance and glucose intolerance–the Chennai Urban Rural Epidemiology Study (CURES). Metabolism. 2006;55(9):1232–8.PubMedCrossRef Deepa R, Velmurugan K, Arvind K, Sivaram P, Sientay C, Uday S, Mohan V. Serum levels of interleukin 6, C-reactive protein, vascular cell adhesion molecule 1, and monocyte chemotactic protein 1 in relation to insulin resistance and glucose intolerance–the Chennai Urban Rural Epidemiology Study (CURES). Metabolism. 2006;55(9):1232–8.PubMedCrossRef
34.
go back to reference Bahceci M, Tuzcu A, Ogun C, Canoruc N, Iltimur K, Aslan C. Is serum C-reactive protein concentration correlated with HbA1c and insulin resistance in Type 2 diabetic men with or without coronary heart disease. J Endocrinol Invest. 2005;28(2):145–50.PubMedCrossRef Bahceci M, Tuzcu A, Ogun C, Canoruc N, Iltimur K, Aslan C. Is serum C-reactive protein concentration correlated with HbA1c and insulin resistance in Type 2 diabetic men with or without coronary heart disease. J Endocrinol Invest. 2005;28(2):145–50.PubMedCrossRef
35.
go back to reference Hwu CM, Lin YC, Lin MW. High levels of C-reactive protein are positively associated with isolated postchallenge hyperglycemia in postmenopausal women. Metab Syndr Relat Disord. 2016;14(7):334–9.PubMedCrossRef Hwu CM, Lin YC, Lin MW. High levels of C-reactive protein are positively associated with isolated postchallenge hyperglycemia in postmenopausal women. Metab Syndr Relat Disord. 2016;14(7):334–9.PubMedCrossRef
36.
go back to reference Carstensen-Kirberg M, Kannenberg JM, Huth C, Meisinger C, Koenig W, Heier M, Peters A, Rathmann W, Roden M, Herder C, et al. Inverse associations between serum levels of secreted frizzled-related protein-5 (SFRP5) and multiple cardiometabolic risk factors: KORA F4 study. Cardiovasc Diabetol. 2017;16(1):109.PubMedPubMedCentralCrossRef Carstensen-Kirberg M, Kannenberg JM, Huth C, Meisinger C, Koenig W, Heier M, Peters A, Rathmann W, Roden M, Herder C, et al. Inverse associations between serum levels of secreted frizzled-related protein-5 (SFRP5) and multiple cardiometabolic risk factors: KORA F4 study. Cardiovasc Diabetol. 2017;16(1):109.PubMedPubMedCentralCrossRef
37.
go back to reference Laakso M. How good a marker is insulin level for insulin resistance. Am J Epidemiol. 1993;137(9):959–65.PubMedCrossRef Laakso M. How good a marker is insulin level for insulin resistance. Am J Epidemiol. 1993;137(9):959–65.PubMedCrossRef
38.
go back to reference Larsen CM, Faulenbach M, Vaag A, Vølund A, Ehses JA, Seifert B, Mandrup-Poulsen T, Donath MY. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med. 2007;356(15):1517–26.PubMedCrossRef Larsen CM, Faulenbach M, Vaag A, Vølund A, Ehses JA, Seifert B, Mandrup-Poulsen T, Donath MY. Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med. 2007;356(15):1517–26.PubMedCrossRef
39.
go back to reference Goldfine AB, Silver R, Aldhahi W, Cai D, Tatro E, Lee J, Shoelson SE. Use of salsalate to target inflammation in the treatment of insulin resistance and type 2 diabetes. Clin Transl Sci. 2008;1(1):36–43.PubMedPubMedCentralCrossRef Goldfine AB, Silver R, Aldhahi W, Cai D, Tatro E, Lee J, Shoelson SE. Use of salsalate to target inflammation in the treatment of insulin resistance and type 2 diabetes. Clin Transl Sci. 2008;1(1):36–43.PubMedPubMedCentralCrossRef
40.
go back to reference Robertson RP, Harmon J, Tran PO, Poitout V. Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes. 2004;53(Suppl 1):S119–24.PubMedCrossRef Robertson RP, Harmon J, Tran PO, Poitout V. Beta-cell glucose toxicity, lipotoxicity, and chronic oxidative stress in type 2 diabetes. Diabetes. 2004;53(Suppl 1):S119–24.PubMedCrossRef
41.
go back to reference Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest. 2006;116(11):3015–25.PubMedPubMedCentralCrossRef Shi H, Kokoeva MV, Inouye K, Tzameli I, Yin H, Flier JS. TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest. 2006;116(11):3015–25.PubMedPubMedCentralCrossRef
42.
go back to reference Hirosumi J, Tuncman G, Chang L, Görgün CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature. 2002;420(6913):333–6.PubMedCrossRef Hirosumi J, Tuncman G, Chang L, Görgün CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature. 2002;420(6913):333–6.PubMedCrossRef
43.
go back to reference Tenenbaum A, Fisman EZ. Mirroring the CANTOS revolution: is anti-inflammatory therapy for diabetes just around the corner. Cardiovasc Diabetol. 2017;16(1):91.PubMedPubMedCentralCrossRef Tenenbaum A, Fisman EZ. Mirroring the CANTOS revolution: is anti-inflammatory therapy for diabetes just around the corner. Cardiovasc Diabetol. 2017;16(1):91.PubMedPubMedCentralCrossRef
44.
go back to reference Lai MM, Li CI, Kardia SL, Liu CS, Lin WY, Lee YD, Chang PC, Lin CC, Li TC. Sex difference in the association of metabolic syndrome with high sensitivity C-reactive protein in a Taiwanese population. BMC Public Health. 2010;10:429.PubMedPubMedCentralCrossRef Lai MM, Li CI, Kardia SL, Liu CS, Lin WY, Lee YD, Chang PC, Lin CC, Li TC. Sex difference in the association of metabolic syndrome with high sensitivity C-reactive protein in a Taiwanese population. BMC Public Health. 2010;10:429.PubMedPubMedCentralCrossRef
45.
go back to reference Hyatt TC, Phadke RP, Hunter GR, Bush NC, Muñoz AJ, Gower BA. Insulin sensitivity in African-American and white women: association with inflammation. Obesity (Silver Spring). 2009;17(2):276–82.CrossRef Hyatt TC, Phadke RP, Hunter GR, Bush NC, Muñoz AJ, Gower BA. Insulin sensitivity in African-American and white women: association with inflammation. Obesity (Silver Spring). 2009;17(2):276–82.CrossRef
46.
go back to reference Khera A, Vega GL, Das SR, Ayers C, McGuire DK, Grundy SM, de Lemos JA. Sex differences in the relationship between C-reactive protein and body fat. J Clin Endocrinol Metab. 2009;94(9):3251–8.PubMedPubMedCentralCrossRef Khera A, Vega GL, Das SR, Ayers C, McGuire DK, Grundy SM, de Lemos JA. Sex differences in the relationship between C-reactive protein and body fat. J Clin Endocrinol Metab. 2009;94(9):3251–8.PubMedPubMedCentralCrossRef
47.
go back to reference Martin BC, Warram JH, Krolewski AS, Bergman RN, Soeldner JS, Kahn CR. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study. Lancet. 1992;340(8825):925–9.PubMedCrossRef Martin BC, Warram JH, Krolewski AS, Bergman RN, Soeldner JS, Kahn CR. Role of glucose and insulin resistance in development of type 2 diabetes mellitus: results of a 25-year follow-up study. Lancet. 1992;340(8825):925–9.PubMedCrossRef
48.
go back to reference Effoe VS, Correa A, Chen H, Lacy ME, Bertoni AG. High-sensitivity C-Reactive protein is associated with incident type 2 diabetes among African Americans: the Jackson Heart Study. Diabetes Care. 2015;38(9):1694–700.PubMedPubMedCentralCrossRef Effoe VS, Correa A, Chen H, Lacy ME, Bertoni AG. High-sensitivity C-Reactive protein is associated with incident type 2 diabetes among African Americans: the Jackson Heart Study. Diabetes Care. 2015;38(9):1694–700.PubMedPubMedCentralCrossRef
Metadata
Title
Temporal relationship between inflammation and insulin resistance and their joint effect on hyperglycemia: the Bogalusa Heart Study
Authors
Yinkun Yan
Shengxu Li
Yang Liu
Lydia Bazzano
Jiang He
Jie Mi
Wei Chen
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2019
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-019-0913-2

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