Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2016

Open Access 01-12-2016 | Original investigation

Circulating angiopoietin-like protein 8 (betatrophin) association with HsCRP and metabolic syndrome

Authors: Mohamed Abu-Farha, Jehad Abubaker, Irina Al-Khairi, Preethi Cherian, Fiona Noronha, Sina Kavalakatt, Abdelkrim Khadir, Kazem Behbehani, Monira Alarouj, Abdullah Bennakhi, Naser Elkum

Published in: Cardiovascular Diabetology | Issue 1/2016

Login to get access

Abstract

Background

ANGPTL8 also called betatrophin is a regulator of lipid metabolism through its interaction with ANGPTL3. It has also been suggested to play a role in insulin resistance and beta-cell proliferation. Based on its function, we hypothesized that ANGPTL8 will play a role in Metabolic Syndrome (MetS). To test this hypothesis we designed this study to measure ANGPTL8 level in subjects with MetS as well as its association with high sensitivity C-reactive protein (HsCRP) level in humans.

Methods

ANGPTL8 level was measured using ELISA in subjects with MetS as well as their controls, a total of 1735 subjects were enrolled. HsCRP was also measured and its association with ANGPTL8 was examined.

Results

ANGPTL8 level was higher in subjects with MetS 1140.6 (171.9–11736.1) pg/mL compared to 710.5 (59.5–11597.2) pg/mL in the controls. Higher levels of ANGPTL8 were also observed with the sequential increase in the number of MetS components (p value = <0.0001). ANGPTL8 showed strong positive correlation with HsCRP (r = 0.15, p value = <0.0001). Stratifying the population into tertiles according to the level of HsCRP showed increased ANGPTL8 level at higher tertiles of HsCRP in the overall population (p value = <0.0001).A similar trend was also observed in MetS and non-MetS subjects as well as in non-obese and obese subjects. Finally, multiple logistic regression models adjusted for age, gender, ethnicity and HsCRP level showed that subjects in the highest tertiles of ANGPTL8 had higher odds of having MetS (odd ratio [OR] = 2.3, 95 % confidence interval [CI] = (1.6–3.1), p value <0.0001.

Conclusion

In this study we showed that ANGPTL8 is increased in subjects with MetS and it was significantly associated with HsCRP levels in different subgroups highlighting its potential role in metabolic and inflammatory pathways.
Literature
1.
go back to reference Mottillo S, Filion KB, Genest J, Joseph L, Pilote L, Poirier P, Rinfret S, Schiffrin EL, Eisenberg MJ. The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol. 2010;56(14):1113–32.CrossRefPubMed Mottillo S, Filion KB, Genest J, Joseph L, Pilote L, Poirier P, Rinfret S, Schiffrin EL, Eisenberg MJ. The metabolic syndrome and cardiovascular risk a systematic review and meta-analysis. J Am Coll Cardiol. 2010;56(14):1113–32.CrossRefPubMed
2.
go back to reference Ballantyne CM, Hoogeveen RC, Bang H, Coresh J, Folsom AR, Chambless LE, Myerson M, Wu KK, Sharrett AR, Boerwinkle E. Lipoprotein-associated phospholipase A2, high-sensitivity C-reactive protein, and risk for incident ischemic stroke in middle-aged men and women in the Atherosclerosis Risk in Communities (ARIC) study. Arch Intern Med. 2005;165(21):2479–84.CrossRefPubMed Ballantyne CM, Hoogeveen RC, Bang H, Coresh J, Folsom AR, Chambless LE, Myerson M, Wu KK, Sharrett AR, Boerwinkle E. Lipoprotein-associated phospholipase A2, high-sensitivity C-reactive protein, and risk for incident ischemic stroke in middle-aged men and women in the Atherosclerosis Risk in Communities (ARIC) study. Arch Intern Med. 2005;165(21):2479–84.CrossRefPubMed
3.
go back to reference Downs JR, Clearfield M, Weis S, Whitney E, Shapiro DR, Beere PA, Langendorfer A, Stein EA, Kruyer W, Gotto AM Jr. Primary prevention of acute coronary events with lovastatin in men and women with average cholesterol levels: results of AFCAPS/TexCAPS. Air Force/Texas Coronary Atherosclerosis Prevention Study. JAMA. 1998;279(20):1615–22.CrossRefPubMed Downs JR, Clearfield M, Weis S, Whitney E, Shapiro DR, Beere PA, Langendorfer A, Stein EA, Kruyer W, Gotto AM Jr. Primary prevention of acute coronary events with lovastatin in men and women with average cholesterol levels: results of AFCAPS/TexCAPS. Air Force/Texas Coronary Atherosclerosis Prevention Study. JAMA. 1998;279(20):1615–22.CrossRefPubMed
4.
go back to reference Rezaianzadeh A, Namayandeh SM, Sadr SM. National Cholesterol Education Program Adult Treatment Panel III Versus International Diabetic Federation Definition of Metabolic Syndrome, Which One is Associated with Diabetes Mellitus and Coronary Artery Disease? Int J Prev Med. 2012;3(8):552–8.PubMedCentralPubMed Rezaianzadeh A, Namayandeh SM, Sadr SM. National Cholesterol Education Program Adult Treatment Panel III Versus International Diabetic Federation Definition of Metabolic Syndrome, Which One is Associated with Diabetes Mellitus and Coronary Artery Disease? Int J Prev Med. 2012;3(8):552–8.PubMedCentralPubMed
5.
go back to reference Parikh R, Mohan V, Joshi S. Should waist circumference be replaced by index of central obesity (ICO) in definition of metabolic syndrome? Diabetes Metab Res Rev. 2012;28(1):3–5.CrossRefPubMed Parikh R, Mohan V, Joshi S. Should waist circumference be replaced by index of central obesity (ICO) in definition of metabolic syndrome? Diabetes Metab Res Rev. 2012;28(1):3–5.CrossRefPubMed
6.
go back to reference Zimmet P, Alberti G. The metabolic syndrome: progress towards one definition for an epidemic of our time. Nat Clin Pract Endocrinol Metab. 2008;4(5):239.CrossRefPubMed Zimmet P, Alberti G. The metabolic syndrome: progress towards one definition for an epidemic of our time. Nat Clin Pract Endocrinol Metab. 2008;4(5):239.CrossRefPubMed
7.
go back to reference Miida T, Seino U, Miyazaki O, Hanyu O, Hirayama S, Saito T, Ishikawa Y, Akamatsu S, Nakano T, Nakajima K, Okazaki M, Okada M. Probucol markedly reduces HDL phospholipids and elevated prebeta1-HDL without delayed conversion into alpha-migrating HDL: putative role of angiopoietin-like protein 3 in probucol-induced HDL remodeling. Atherosclerosis. 2008;200(2):329–35.CrossRefPubMed Miida T, Seino U, Miyazaki O, Hanyu O, Hirayama S, Saito T, Ishikawa Y, Akamatsu S, Nakano T, Nakajima K, Okazaki M, Okada M. Probucol markedly reduces HDL phospholipids and elevated prebeta1-HDL without delayed conversion into alpha-migrating HDL: putative role of angiopoietin-like protein 3 in probucol-induced HDL remodeling. Atherosclerosis. 2008;200(2):329–35.CrossRefPubMed
8.
go back to reference Yudkin JS, Juhan-Vague I, Hawe E, Humphries SE, di Minno G, Margaglione M, Tremoli E, Kooistra T, Morange PE, Lundman P, Mohamed-Ali V, Hamsten A. Low-grade inflammation may play a role in the etiology of the metabolic syndrome in patients with coronary heart disease: the HIFMECH study. Metabolism. 2004;53(7):852–7.CrossRefPubMed Yudkin JS, Juhan-Vague I, Hawe E, Humphries SE, di Minno G, Margaglione M, Tremoli E, Kooistra T, Morange PE, Lundman P, Mohamed-Ali V, Hamsten A. Low-grade inflammation may play a role in the etiology of the metabolic syndrome in patients with coronary heart disease: the HIFMECH study. Metabolism. 2004;53(7):852–7.CrossRefPubMed
9.
go back to reference Povel CM, Beulens JW, van der Schouw YT, Dolle ME, Spijkerman AM, Verschuren WM, Feskens EJ, Boer JM. Metabolic syndrome model definitions predicting type 2 diabetes and cardiovascular disease. Diabetes Care. 2013;36(2):362–8.PubMedCentralCrossRefPubMed Povel CM, Beulens JW, van der Schouw YT, Dolle ME, Spijkerman AM, Verschuren WM, Feskens EJ, Boer JM. Metabolic syndrome model definitions predicting type 2 diabetes and cardiovascular disease. Diabetes Care. 2013;36(2):362–8.PubMedCentralCrossRefPubMed
10.
go back to reference Rodriguez-Leal GA, Moran S, Gallardo I, Milke P, Guevara-Gonzalez L. Assessment of high sensitivity C-reactive protein (HS-CRP) as a marker of liver inflammation in patients with metabolic syndrome. Rev Gastroenterol Mex. 2006;71(1):39–45.PubMed Rodriguez-Leal GA, Moran S, Gallardo I, Milke P, Guevara-Gonzalez L. Assessment of high sensitivity C-reactive protein (HS-CRP) as a marker of liver inflammation in patients with metabolic syndrome. Rev Gastroenterol Mex. 2006;71(1):39–45.PubMed
11.
go back to reference Rasouli M, Kiasari AM. Interactions of serum hsCRP with apoB, apoB/AI ratio and some components of metabolic syndrome amplify the predictive values for coronary artery disease. Clin Biochem. 2006;39(10):971–7.CrossRefPubMed Rasouli M, Kiasari AM. Interactions of serum hsCRP with apoB, apoB/AI ratio and some components of metabolic syndrome amplify the predictive values for coronary artery disease. Clin Biochem. 2006;39(10):971–7.CrossRefPubMed
12.
go back to reference Devaraj S, Swarbrick MM, Singh U, Adams-Huet B, Havel PJ, Jialal I. CRP and adiponectin and its oligomers in the metabolic syndrome: evaluation of new laboratory-based biomarkers. Am J Clin Pathol. 2008;129(5):815–22.PubMedCentralCrossRefPubMed Devaraj S, Swarbrick MM, Singh U, Adams-Huet B, Havel PJ, Jialal I. CRP and adiponectin and its oligomers in the metabolic syndrome: evaluation of new laboratory-based biomarkers. Am J Clin Pathol. 2008;129(5):815–22.PubMedCentralCrossRefPubMed
14.
go back to reference Ren G, Kim JY, Smas CM. Identification of RIFL, a novel adipocyte-enriched insulin target gene with a role in lipid metabolism. Am J Physiol Endocrinol Metab. 2012;303(3):E334–51.PubMedCentralCrossRefPubMed Ren G, Kim JY, Smas CM. Identification of RIFL, a novel adipocyte-enriched insulin target gene with a role in lipid metabolism. Am J Physiol Endocrinol Metab. 2012;303(3):E334–51.PubMedCentralCrossRefPubMed
15.
go back to reference Quagliarini F, Wang Y, Kozlitina J, Grishin NV, Hyde R, Boerwinkle E, Valenzuela DM, Murphy AJ, Cohen JC, Hobbs HH. Atypical angiopoietin-like protein that regulates ANGPTL3. Proc Natl Acad Sci USA. 2012;109(48):19751–6.PubMedCentralCrossRefPubMed Quagliarini F, Wang Y, Kozlitina J, Grishin NV, Hyde R, Boerwinkle E, Valenzuela DM, Murphy AJ, Cohen JC, Hobbs HH. Atypical angiopoietin-like protein that regulates ANGPTL3. Proc Natl Acad Sci USA. 2012;109(48):19751–6.PubMedCentralCrossRefPubMed
16.
go back to reference Zhang R, Abou-Samra AB. Emerging roles of Lipasin as a critical lipid regulator. Biochem Biophys Res Commun. 2013;432(3):401–5.CrossRefPubMed Zhang R, Abou-Samra AB. Emerging roles of Lipasin as a critical lipid regulator. Biochem Biophys Res Commun. 2013;432(3):401–5.CrossRefPubMed
17.
go back to reference Zhang R. Lipasin, a novel nutritionally-regulated liver-enriched factor that regulates serum triglyceride levels. Biochem Biophys Res Commun. 2012;424(4):786–92.CrossRefPubMed Zhang R. Lipasin, a novel nutritionally-regulated liver-enriched factor that regulates serum triglyceride levels. Biochem Biophys Res Commun. 2012;424(4):786–92.CrossRefPubMed
18.
go back to reference Abubaker J, Tiss A, Abu-Farha M, Al-Ghimlas F, Al-Khairi I, Baturcam E, Cherian P, Elkum N, Hammad M, John J, Kavalakatt S, Khadir A, Warsame S, Dermime S, Behbehani K, Dehbi M. DNAJB3/HSP-40 cochaperone is downregulated in obese humans and is restored by physical exercise. PLoS One. 2013;8(7):e69217.PubMedCentralCrossRefPubMed Abubaker J, Tiss A, Abu-Farha M, Al-Ghimlas F, Al-Khairi I, Baturcam E, Cherian P, Elkum N, Hammad M, John J, Kavalakatt S, Khadir A, Warsame S, Dermime S, Behbehani K, Dehbi M. DNAJB3/HSP-40 cochaperone is downregulated in obese humans and is restored by physical exercise. PLoS One. 2013;8(7):e69217.PubMedCentralCrossRefPubMed
19.
go back to reference Gusarova V, Alexa CA, Na E, Stevis PE, Xin Y, Bonner-Weir S, Cohen JC, Hobbs HH, Murphy AJ, Yancopoulos GD, Gromada J. ANGPTL8/betatrophin does not control pancreatic beta cell expansion. Cell. 2014;159(3):691–6.PubMedCentralCrossRefPubMed Gusarova V, Alexa CA, Na E, Stevis PE, Xin Y, Bonner-Weir S, Cohen JC, Hobbs HH, Murphy AJ, Yancopoulos GD, Gromada J. ANGPTL8/betatrophin does not control pancreatic beta cell expansion. Cell. 2014;159(3):691–6.PubMedCentralCrossRefPubMed
20.
go back to reference Yi P, Park JS, Melton DA. Perspectives on the activities of ANGPTL8/betatrophin. Cell. 2014;159(3):467–8.CrossRefPubMed Yi P, Park JS, Melton DA. Perspectives on the activities of ANGPTL8/betatrophin. Cell. 2014;159(3):467–8.CrossRefPubMed
21.
go back to reference Abu-Farha M, Abubaker J, Al-Khairi I, Cherian P, Noronha F, Hu FB, Behbehani K, Elkum N. Higher plasma betatrophin/ANGPTL8 level in Type 2 Diabetes subjects does not correlate with blood glucose or insulin resistance. Sci Rep. 2015;5:10949.PubMedCentralCrossRefPubMed Abu-Farha M, Abubaker J, Al-Khairi I, Cherian P, Noronha F, Hu FB, Behbehani K, Elkum N. Higher plasma betatrophin/ANGPTL8 level in Type 2 Diabetes subjects does not correlate with blood glucose or insulin resistance. Sci Rep. 2015;5:10949.PubMedCentralCrossRefPubMed
22.
go back to reference Abu-Farha M, Abubaker J, Noronha F, Al-Khairi I, Cherian P, Alarouj M, Bennakhi A, Elkum N. Lack of associations between betatrophin/ANGPTL8 level and C-peptide in type 2 diabetic subjects. Cardiovasc Diabetol. 2015;14:112.PubMedCentralCrossRefPubMed Abu-Farha M, Abubaker J, Noronha F, Al-Khairi I, Cherian P, Alarouj M, Bennakhi A, Elkum N. Lack of associations between betatrophin/ANGPTL8 level and C-peptide in type 2 diabetic subjects. Cardiovasc Diabetol. 2015;14:112.PubMedCentralCrossRefPubMed
23.
go back to reference Abu-Farha M, Behbehani K, Elkum N. Comprehensive analysis of circulating adipokines and hsCRP association with cardiovascular disease risk factors and metabolic syndrome in Arabs. Cardiovasc Diabetol. 2014;13:76.PubMedCentralCrossRefPubMed Abu-Farha M, Behbehani K, Elkum N. Comprehensive analysis of circulating adipokines and hsCRP association with cardiovascular disease risk factors and metabolic syndrome in Arabs. Cardiovasc Diabetol. 2014;13:76.PubMedCentralCrossRefPubMed
24.
go back to reference Diagnosis and classification of diabetes mellitus. Diabetes Care. 2008;31(Suppl 1):S55–60. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2008;31(Suppl 1):S55–60.
25.
go back to reference Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, Jones DW, Materson BJ, Oparil S, Wright JT Jr, Roccella EJ. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA. 2003;289(19):2560–72.CrossRefPubMed Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, Jones DW, Materson BJ, Oparil S, Wright JT Jr, Roccella EJ. The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA. 2003;289(19):2560–72.CrossRefPubMed
26.
go back to reference Li Y, Teng C. Angiopoietin-like proteins 3, 4 and 8: regulating lipid metabolism and providing new hope for metabolic syndrome. J Drug Target. 2014;22(8):679–87.CrossRefPubMed Li Y, Teng C. Angiopoietin-like proteins 3, 4 and 8: regulating lipid metabolism and providing new hope for metabolic syndrome. J Drug Target. 2014;22(8):679–87.CrossRefPubMed
27.
go back to reference Santulli G. Angiopoietin-like proteins: a comprehensive look. Front Endocrinol (Lausanne). 2014;5:4. Santulli G. Angiopoietin-like proteins: a comprehensive look. Front Endocrinol (Lausanne). 2014;5:4.
28.
go back to reference Kadomatsu T, Tabata M, Oike Y. Angiopoietin-like proteins: emerging targets for treatment of obesity and related metabolic diseases. FEBS J. 2011;278(4):559–64.CrossRefPubMed Kadomatsu T, Tabata M, Oike Y. Angiopoietin-like proteins: emerging targets for treatment of obesity and related metabolic diseases. FEBS J. 2011;278(4):559–64.CrossRefPubMed
29.
go back to reference Oike Y, Akao M, Kubota Y, Suda T. Angiopoietin-like proteins: potential new targets for metabolic syndrome therapy. Trends Mol Med. 2005;11(10):473–9.CrossRefPubMed Oike Y, Akao M, Kubota Y, Suda T. Angiopoietin-like proteins: potential new targets for metabolic syndrome therapy. Trends Mol Med. 2005;11(10):473–9.CrossRefPubMed
30.
go back to reference Zhang R, Abou-Samra AB. A dual role of lipasin (betatrophin) in lipid metabolism and glucose homeostasis: consensus and controversy. Cardiovasc Diabetol. 2014;13:133.PubMedCentralCrossRefPubMed Zhang R, Abou-Samra AB. A dual role of lipasin (betatrophin) in lipid metabolism and glucose homeostasis: consensus and controversy. Cardiovasc Diabetol. 2014;13:133.PubMedCentralCrossRefPubMed
31.
go back to reference Espes D, Martinell M, Carlsson PO. Increased circulating betatrophin concentrations in patients with type 2 diabetes. Int J Endocrinol. 2014;2014:323407.PubMedCentralCrossRefPubMed Espes D, Martinell M, Carlsson PO. Increased circulating betatrophin concentrations in patients with type 2 diabetes. Int J Endocrinol. 2014;2014:323407.PubMedCentralCrossRefPubMed
32.
go back to reference Fu Z, Berhane F, Fite A, Seyoum B, Abou-Samra AB, Zhang R. Elevated circulating lipasin/betatrophin in human type 2 diabetes and obesity. Sci Rep. 2014;4:5013.PubMed Fu Z, Berhane F, Fite A, Seyoum B, Abou-Samra AB, Zhang R. Elevated circulating lipasin/betatrophin in human type 2 diabetes and obesity. Sci Rep. 2014;4:5013.PubMed
33.
go back to reference Hu H, Sun W, Yu S, Hong X, Qian W, Tang B, Wang D, Yang L, Wang J, Mao C, Zhou L. Increased circulating levels of betatrophin in newly diagnosed type 2 diabetic patients. Diabetes Care. 2014;37(10):2718–22.CrossRefPubMed Hu H, Sun W, Yu S, Hong X, Qian W, Tang B, Wang D, Yang L, Wang J, Mao C, Zhou L. Increased circulating levels of betatrophin in newly diagnosed type 2 diabetic patients. Diabetes Care. 2014;37(10):2718–22.CrossRefPubMed
34.
go back to reference Gao T, Jin K, Chen P, Jin H, Yang L, Xie X, Yang M, Hu C, Yu X. Circulating Betatrophin Correlates with Triglycerides and Postprandial Glucose among Different Glucose Tolerance Statuses–a Case-Control Study. PLoS One. 2015;10(8):e0133640.PubMedCentralCrossRefPubMed Gao T, Jin K, Chen P, Jin H, Yang L, Xie X, Yang M, Hu C, Yu X. Circulating Betatrophin Correlates with Triglycerides and Postprandial Glucose among Different Glucose Tolerance Statuses–a Case-Control Study. PLoS One. 2015;10(8):e0133640.PubMedCentralCrossRefPubMed
35.
go back to reference Gokulakrishnan K, Manokaran K, Pandey GK, Amutha A, Ranjani H, Anjana RM, Mohan V. Relationship of betatrophin with youth onset type 2 diabetes among Asian Indians. Diabetes Res Clin Pract. 2015;109(1):71–6.CrossRefPubMed Gokulakrishnan K, Manokaran K, Pandey GK, Amutha A, Ranjani H, Anjana RM, Mohan V. Relationship of betatrophin with youth onset type 2 diabetes among Asian Indians. Diabetes Res Clin Pract. 2015;109(1):71–6.CrossRefPubMed
36.
go back to reference Gómez-Ambrosi J, Pascual E, Catalán V, Rodríguez A, Ramírez B, Silva C, Gil MJ, Salvador J, Frühbeck G. Circulating betatrophin concentrations are decreased in human obesity and type 2 diabetes. J Clin Endocrinol Metab. 2014;99(10):E2004–9.CrossRefPubMed Gómez-Ambrosi J, Pascual E, Catalán V, Rodríguez A, Ramírez B, Silva C, Gil MJ, Salvador J, Frühbeck G. Circulating betatrophin concentrations are decreased in human obesity and type 2 diabetes. J Clin Endocrinol Metab. 2014;99(10):E2004–9.CrossRefPubMed
37.
go back to reference Alberti KG, Zimmet P, Shaw J. The metabolic syndrome–a new worldwide definition. Lancet. 2005;366(9491):1059–62.CrossRefPubMed Alberti KG, Zimmet P, Shaw J. The metabolic syndrome–a new worldwide definition. Lancet. 2005;366(9491):1059–62.CrossRefPubMed
38.
go back to reference Devaraj S, Valleggi S, Siegel D, Jialal I. Role of C-reactive protein in contributing to increased cardiovascular risk in metabolic syndrome. Curr Atheroscler Rep. 2010;12(2):110–8.PubMedCentralCrossRefPubMed Devaraj S, Valleggi S, Siegel D, Jialal I. Role of C-reactive protein in contributing to increased cardiovascular risk in metabolic syndrome. Curr Atheroscler Rep. 2010;12(2):110–8.PubMedCentralCrossRefPubMed
39.
40.
go back to reference Abu-Farha M, Sriraman D, Cherian P, AlKhairi I, Elkum N, Behbehani K, Abubaker J. Circulating ANGPTL8/Betatrophin Is Increased in Obesity and Reduced after Exercise Training. PLoS One. 2016;11(1):e0147367.PubMedCentralCrossRefPubMed Abu-Farha M, Sriraman D, Cherian P, AlKhairi I, Elkum N, Behbehani K, Abubaker J. Circulating ANGPTL8/Betatrophin Is Increased in Obesity and Reduced after Exercise Training. PLoS One. 2016;11(1):e0147367.PubMedCentralCrossRefPubMed
41.
go back to reference Fu Z, Abou-Samra AB, Zhang R. An explanation for recent discrepancies in levels of human circulating betatrophin. Diabetologia. 2014;57(10):2232–4.CrossRefPubMed Fu Z, Abou-Samra AB, Zhang R. An explanation for recent discrepancies in levels of human circulating betatrophin. Diabetologia. 2014;57(10):2232–4.CrossRefPubMed
42.
go back to reference Tjeerdema N, Georgiadi A, Jonker JT, van Glabbeek M. Alizadeh Dehnavi R, Tamsma JT, Smit JW, Kersten S, Rensen PC: Inflammation increases plasma angiopoietin-like protein 4 in patients with the metabolic syndrome and type 2 diabetes. BMJ Open Diabetes Res Care. 2014;2(1):e000034.PubMedCentralCrossRefPubMed Tjeerdema N, Georgiadi A, Jonker JT, van Glabbeek M. Alizadeh Dehnavi R, Tamsma JT, Smit JW, Kersten S, Rensen PC: Inflammation increases plasma angiopoietin-like protein 4 in patients with the metabolic syndrome and type 2 diabetes. BMJ Open Diabetes Res Care. 2014;2(1):e000034.PubMedCentralCrossRefPubMed
43.
go back to reference Mehta N, Qamar A, Qu L, Qasim AN, Mehta NN, Reilly MP, Rader DJ. Differential association of plasma angiopoietin-like proteins 3 and 4 with lipid and metabolic traits. Arterioscler Thromb Vasc Biol. 2014;34(5):1057–63.PubMedCentralCrossRefPubMed Mehta N, Qamar A, Qu L, Qasim AN, Mehta NN, Reilly MP, Rader DJ. Differential association of plasma angiopoietin-like proteins 3 and 4 with lipid and metabolic traits. Arterioscler Thromb Vasc Biol. 2014;34(5):1057–63.PubMedCentralCrossRefPubMed
Metadata
Title
Circulating angiopoietin-like protein 8 (betatrophin) association with HsCRP and metabolic syndrome
Authors
Mohamed Abu-Farha
Jehad Abubaker
Irina Al-Khairi
Preethi Cherian
Fiona Noronha
Sina Kavalakatt
Abdelkrim Khadir
Kazem Behbehani
Monira Alarouj
Abdullah Bennakhi
Naser Elkum
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2016
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/s12933-016-0346-0

Other articles of this Issue 1/2016

Cardiovascular Diabetology 1/2016 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine