Skip to main content
Top
Published in: Cardiovascular Diabetology 1/2013

Open Access 01-12-2013 | Original investigation

High sensitive C-reactive protein and serum amyloid A are inversely related to serum bilirubin: effect-modification by metabolic syndrome

Authors: Petronella E Deetman, Stephan JL Bakker, Robin PF Dullaart

Published in: Cardiovascular Diabetology | Issue 1/2013

Login to get access

Abstract

Background

Bilirubin has been implicated in cardiovascular protection by virtue of its anti-inflammatory and anti-oxidative properties. The metabolic syndrome is featured by enhanced low-grade systemic inflammation and oxidative stress. Serum amyloid A (SAA) impairs anti-oxidative properties of high-density lipoprotein (HDL). We determined relationships of high sensitive C-reactive protein (hs-CRP) and SAA with bilirubin in subjects with and without metabolic syndrome (MetS).

Methods

Serum total bilirubin, hs-CRP, SAA and homeostasis model assessment- insulin resistance (HOMA-IR) were documented in 94 subjects with and in 73 subjects without MetS (26 and 54 subjects with type 2 diabetes mellitus (T2DM), respectively).

Results

Bilirubin was lower in MetS (P = 0.013), coinciding with higher hs-CRP (P < 0.001) and SAA levels (P = 0.002). In all subjects combined, hs-CRP was inversely related to bilirubin (r = −0.203, P = 0.008), irrespective of the presence of MetS or T2DM (interaction terms: P ≥ 0.75). The inverse relationship of bilirubin with SAA was confined to subjects without MetS (r = −0.267, P = 0.009). Furthermore, the presence of either MetS or T2DM modified the relationship of bilirubin with SAA (interaction terms: β = 0.366, P = 0.003 and β = 0.289, P = 0.025, respectively) in age- and sex-adjusted analyses. Effect modification was also found for HOMA-IR (β = 0.790, P = 0.020). Of the individual MetS components, the strongest interaction of bilirubin on SAA was observed with low HDL cholesterol (β = 0.435, P < 0.001).

Conclusions

hs-CRP is inversely related to bilirubin, suggesting that low bilirubin is implicated in enhanced low-grade systemic inflammation. The inverse relationship of SAA with bilirubin was found to be absent in MetS, which could be attributable to MetS-associated abnormalities in HDL characteristics.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mazzone GL, Rigato I, Ostrow JD, Bossi F, Bortoluzzi A, Sukowati CH, Tedesco F, Tiribelli C: Bilirubin inhibits the TNFalpha-related induction of three endothelial adhesion molecules. Biochem Biophys Res Commun. 2009, 386 (2): 338-344. 10.1016/j.bbrc.2009.06.029.CrossRefPubMed Mazzone GL, Rigato I, Ostrow JD, Bossi F, Bortoluzzi A, Sukowati CH, Tedesco F, Tiribelli C: Bilirubin inhibits the TNFalpha-related induction of three endothelial adhesion molecules. Biochem Biophys Res Commun. 2009, 386 (2): 338-344. 10.1016/j.bbrc.2009.06.029.CrossRefPubMed
2.
go back to reference Abraham NG, Kappas A: Heme oxygenase and the cardiovascular-renal system. Free Radic Biol Med. 2005, 39 (1): 1-25. 10.1016/j.freeradbiomed.2005.03.010.CrossRefPubMed Abraham NG, Kappas A: Heme oxygenase and the cardiovascular-renal system. Free Radic Biol Med. 2005, 39 (1): 1-25. 10.1016/j.freeradbiomed.2005.03.010.CrossRefPubMed
4.
go back to reference Hansel B, Giral P, Nobecourt E, Chantepie S, Bruckert E, Chapman MJ, Kontush A: Metabolic syndrome is associated with elevated oxidative stress and dysfunctional dense high-density lipoprotein particles displaying impaired antioxidative activity. J Clin Endocrinol Metab. 2004, 89 (10): 4963-4971. 10.1210/jc.2004-0305.CrossRefPubMed Hansel B, Giral P, Nobecourt E, Chantepie S, Bruckert E, Chapman MJ, Kontush A: Metabolic syndrome is associated with elevated oxidative stress and dysfunctional dense high-density lipoprotein particles displaying impaired antioxidative activity. J Clin Endocrinol Metab. 2004, 89 (10): 4963-4971. 10.1210/jc.2004-0305.CrossRefPubMed
5.
go back to reference Choi SH, Yun KE, Choi HJ: Relationships between serum total bilirubin levels and metabolic syndrome in Korean adults. Nutr Metab Cardiovasc Dis. 2013, 23 (1): 31-37. 10.1016/j.numecd.2011.03.001.CrossRefPubMed Choi SH, Yun KE, Choi HJ: Relationships between serum total bilirubin levels and metabolic syndrome in Korean adults. Nutr Metab Cardiovasc Dis. 2013, 23 (1): 31-37. 10.1016/j.numecd.2011.03.001.CrossRefPubMed
6.
go back to reference Robertson RP, Harmon JS: Diabetes, glucose toxicity, and oxidative stress: A case of double jeopardy for the pancreatic islet beta cell. Free Radic Biol Med. 2006, 41 (2): 177-184. 10.1016/j.freeradbiomed.2005.04.030.CrossRefPubMed Robertson RP, Harmon JS: Diabetes, glucose toxicity, and oxidative stress: A case of double jeopardy for the pancreatic islet beta cell. Free Radic Biol Med. 2006, 41 (2): 177-184. 10.1016/j.freeradbiomed.2005.04.030.CrossRefPubMed
7.
go back to reference Kim KM, Kim BT, Park SB, Cho DY, Je SH, Kim KN: Serum total bilirubin concentration is inversely correlated with Framingham risk score in Koreans. Arch Med Res. 2012, 43 (4): 288-293. 10.1016/j.arcmed.2012.05.003.CrossRefPubMed Kim KM, Kim BT, Park SB, Cho DY, Je SH, Kim KN: Serum total bilirubin concentration is inversely correlated with Framingham risk score in Koreans. Arch Med Res. 2012, 43 (4): 288-293. 10.1016/j.arcmed.2012.05.003.CrossRefPubMed
8.
go back to reference Kang SJ, Kim D, Park HE, Chung GE, Choi SH, Choi SY, Lee W, Kim JS, Cho SH: Elevated serum bilirubin levels are inversely associated with coronary artery atherosclerosis. Atherosclerosis. 2013, 230 (2): 242-248. 10.1016/j.atherosclerosis.2013.06.021.CrossRefPubMed Kang SJ, Kim D, Park HE, Chung GE, Choi SH, Choi SY, Lee W, Kim JS, Cho SH: Elevated serum bilirubin levels are inversely associated with coronary artery atherosclerosis. Atherosclerosis. 2013, 230 (2): 242-248. 10.1016/j.atherosclerosis.2013.06.021.CrossRefPubMed
9.
go back to reference Vitek L, Novotny L, Sperl M, Holaj R, Spacil J: The inverse association of elevated serum bilirubin levels with subclinical carotid atherosclerosis. Cerebrovasc Dis. 2006, 21 (5–6): 408-414.PubMed Vitek L, Novotny L, Sperl M, Holaj R, Spacil J: The inverse association of elevated serum bilirubin levels with subclinical carotid atherosclerosis. Cerebrovasc Dis. 2006, 21 (5–6): 408-414.PubMed
10.
go back to reference Yoshino S, Hamasaki S, Ishida S, Kataoka T, Yoshikawa A, Oketani N, Saihara K, Okui H, Shinsato T, Ichiki H, Kubozono T, Kuwahata S, Fujita S, Kanda D, Nakazaki M, Miyata M, Tei C: Relationship between bilirubin concentration, coronary endothelial function, and inflammatory stress in overweight patients. J Atheroscler Thromb. 2011, 18 (5): 403-412. 10.5551/jat.6346.CrossRefPubMed Yoshino S, Hamasaki S, Ishida S, Kataoka T, Yoshikawa A, Oketani N, Saihara K, Okui H, Shinsato T, Ichiki H, Kubozono T, Kuwahata S, Fujita S, Kanda D, Nakazaki M, Miyata M, Tei C: Relationship between bilirubin concentration, coronary endothelial function, and inflammatory stress in overweight patients. J Atheroscler Thromb. 2011, 18 (5): 403-412. 10.5551/jat.6346.CrossRefPubMed
11.
go back to reference Dullaart RP, Kappelle PJ, De Vries R: Lower carotid intima media thickness is predicted by higher serum bilirubin in both non-diabetic and Type 2 diabetic subjects. Clin Chim Acta. 2012, 414: 161-165.CrossRefPubMed Dullaart RP, Kappelle PJ, De Vries R: Lower carotid intima media thickness is predicted by higher serum bilirubin in both non-diabetic and Type 2 diabetic subjects. Clin Chim Acta. 2012, 414: 161-165.CrossRefPubMed
12.
go back to reference Novotny L, Vitek L: Inverse relationship between serum bilirubin and atherosclerosis in men: a meta-analysis of published studies. Exp Biol Med (Maywood). 2003, 228 (5): 568-571. Novotny L, Vitek L: Inverse relationship between serum bilirubin and atherosclerosis in men: a meta-analysis of published studies. Exp Biol Med (Maywood). 2003, 228 (5): 568-571.
13.
go back to reference Chan KH, O’Connell RL, Sullivan DR, Hoffmann LS, Rajamani K, Whiting M, Donoghoe MW, Vanhala M, Hamer A, Yu B, Stocker R, Ng MK, Keech AC: FIELD study investigators: plasma total Bilirubin levels predict amputation events in type 2 diabetes mellitus: the Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) study. Diabetologia. 2013, 56 (4): 724-736. 10.1007/s00125-012-2818-4.CrossRefPubMed Chan KH, O’Connell RL, Sullivan DR, Hoffmann LS, Rajamani K, Whiting M, Donoghoe MW, Vanhala M, Hamer A, Yu B, Stocker R, Ng MK, Keech AC: FIELD study investigators: plasma total Bilirubin levels predict amputation events in type 2 diabetes mellitus: the Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) study. Diabetologia. 2013, 56 (4): 724-736. 10.1007/s00125-012-2818-4.CrossRefPubMed
14.
go back to reference Ajja R, Lee DC, Sui X, Church TS, Steven NB: Usefulness of serum Bilirubin and cardiorespiratory fitness as predictors of mortality in men. Am J Cardiol. 2011, 108 (10): 1438-1442. 10.1016/j.amjcard.2011.06.067.PubMedCentralCrossRefPubMed Ajja R, Lee DC, Sui X, Church TS, Steven NB: Usefulness of serum Bilirubin and cardiorespiratory fitness as predictors of mortality in men. Am J Cardiol. 2011, 108 (10): 1438-1442. 10.1016/j.amjcard.2011.06.067.PubMedCentralCrossRefPubMed
15.
go back to reference Vitek L, Schwertner HA: The heme catabolic pathway and its protective effects on oxidative stress-mediated diseases. Adv Clin Chem. 2007, 43: 1-57.CrossRefPubMed Vitek L, Schwertner HA: The heme catabolic pathway and its protective effects on oxidative stress-mediated diseases. Adv Clin Chem. 2007, 43: 1-57.CrossRefPubMed
16.
go back to reference Hwang HJ, Lee SW, Kim SH: Relationship between Bilirubin and C-reactive protein. Clin Chem Lab Med. 2011, 49 (11): 1823-1828.CrossRefPubMed Hwang HJ, Lee SW, Kim SH: Relationship between Bilirubin and C-reactive protein. Clin Chem Lab Med. 2011, 49 (11): 1823-1828.CrossRefPubMed
17.
go back to reference Wallner M, Marculescu R, Doberer D, Wolzt M, Wagner O, Vitek L, Bulmer AC, Wagner KH: Protection from age-related increase in lipid biomarkers and inflammation contributes to cardiovascular protection in Gilbert’s syndrome. Clin Sci (Lond). 2013, 125 (5): 257-264. 10.1042/CS20120661.CrossRef Wallner M, Marculescu R, Doberer D, Wolzt M, Wagner O, Vitek L, Bulmer AC, Wagner KH: Protection from age-related increase in lipid biomarkers and inflammation contributes to cardiovascular protection in Gilbert’s syndrome. Clin Sci (Lond). 2013, 125 (5): 257-264. 10.1042/CS20120661.CrossRef
18.
go back to reference Dullaart RP, De Boer JF, Annema W, Tietge UJ: The inverse relation of HDL anti-oxidative functionality with serum amyloid a is lost in metabolic syndrome subjects. Obesity (Silver Spring). 2013, 21 (2): 361-366. 10.1002/oby.20058.CrossRef Dullaart RP, De Boer JF, Annema W, Tietge UJ: The inverse relation of HDL anti-oxidative functionality with serum amyloid a is lost in metabolic syndrome subjects. Obesity (Silver Spring). 2013, 21 (2): 361-366. 10.1002/oby.20058.CrossRef
19.
go back to reference Kontush A, Chapman MJ: Functionally defective high-density lipoprotein: a new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis. Pharmacol Rev. 2006, 58 (3): 342-374. 10.1124/pr.58.3.1.CrossRefPubMed Kontush A, Chapman MJ: Functionally defective high-density lipoprotein: a new therapeutic target at the crossroads of dyslipidemia, inflammation, and atherosclerosis. Pharmacol Rev. 2006, 58 (3): 342-374. 10.1124/pr.58.3.1.CrossRefPubMed
20.
go back to reference Nofer J: Serum amyloid A concentration may reflect HDL functionality. Clin Lipidol. in press Nofer J: Serum amyloid A concentration may reflect HDL functionality. Clin Lipidol. in press
21.
go back to reference Ridker PM, Hennekens CH, Buring JE, Rifai N: C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000, 342 (12): 836-843. 10.1056/NEJM200003233421202.CrossRefPubMed Ridker PM, Hennekens CH, Buring JE, Rifai N: C-reactive protein and other markers of inflammation in the prediction of cardiovascular disease in women. N Engl J Med. 2000, 342 (12): 836-843. 10.1056/NEJM200003233421202.CrossRefPubMed
22.
go back to reference Danesh J, Whincup P, Walker M, Lennon L, Thomson A, Appleby P, Gallimore JR, Pepys MB: Low grade inflammation and coronary heart disease: prospective study and updated meta-analyses. BMJ. 2000, 321 (7255): 199-204. 10.1136/bmj.321.7255.199.PubMedCentralCrossRefPubMed Danesh J, Whincup P, Walker M, Lennon L, Thomson A, Appleby P, Gallimore JR, Pepys MB: Low grade inflammation and coronary heart disease: prospective study and updated meta-analyses. BMJ. 2000, 321 (7255): 199-204. 10.1136/bmj.321.7255.199.PubMedCentralCrossRefPubMed
23.
go back to reference Johnson BD, Kip KE, Marroquin OC, Ridker PM, Kelsey SF, Shaw LJ, Pepine CJ, Sharaf B, Bairey Merz CN, Sopko G, Olson MB, Reis SE: National Heart, Lung, and Blood Institute: Serum amyloid A as a predictor of coronary artery disease and cardiovascular outcome in women: the National Heart, Lung, and Blood Institute-Sponsored Women’s Ischemia Syndrome Evaluation (WISE). Circulation. 2004, 109 (6): 726-732. 10.1161/01.CIR.0000115516.54550.B1.CrossRefPubMed Johnson BD, Kip KE, Marroquin OC, Ridker PM, Kelsey SF, Shaw LJ, Pepine CJ, Sharaf B, Bairey Merz CN, Sopko G, Olson MB, Reis SE: National Heart, Lung, and Blood Institute: Serum amyloid A as a predictor of coronary artery disease and cardiovascular outcome in women: the National Heart, Lung, and Blood Institute-Sponsored Women’s Ischemia Syndrome Evaluation (WISE). Circulation. 2004, 109 (6): 726-732. 10.1161/01.CIR.0000115516.54550.B1.CrossRefPubMed
24.
go back to reference Kappelle PJ, Bijzet J, Hazenberg BP, Dullaart RP: Lower serum paraoxonase-1 activity is related to higher serum amyloid a levels in metabolic syndrome. Arch Med Res. 2011, 42 (3): 219-225. 10.1016/j.arcmed.2011.05.002.CrossRefPubMed Kappelle PJ, Bijzet J, Hazenberg BP, Dullaart RP: Lower serum paraoxonase-1 activity is related to higher serum amyloid a levels in metabolic syndrome. Arch Med Res. 2011, 42 (3): 219-225. 10.1016/j.arcmed.2011.05.002.CrossRefPubMed
25.
go back to reference Jylhava J, Haarala A, Eklund C, Pertovaara M, Kahonen M, Hutri-Kahonen N, Levula M, Lehtimaki T, Huupponen R, Jula A, Juonala M, Viikari J, Raitakari O, Hurme M: Serum amyloid a is independently associated with metabolic risk factors but not with early atherosclerosis: the cardiovascular risk in young Finns study. J Intern Med. 2009, 266 (3): 286-295. 10.1111/j.1365-2796.2009.02120.x.CrossRefPubMed Jylhava J, Haarala A, Eklund C, Pertovaara M, Kahonen M, Hutri-Kahonen N, Levula M, Lehtimaki T, Huupponen R, Jula A, Juonala M, Viikari J, Raitakari O, Hurme M: Serum amyloid a is independently associated with metabolic risk factors but not with early atherosclerosis: the cardiovascular risk in young Finns study. J Intern Med. 2009, 266 (3): 286-295. 10.1111/j.1365-2796.2009.02120.x.CrossRefPubMed
26.
go back to reference Den Engelsen C, Koekkoek PS, Gorter KJ, Van den Donk M, Salome PL, Rutten GE: High-sensitivity C-reactive protein to detect metabolic syndrome in a centrally obese population: a cross-sectional analysis. Cardiovasc Diabetol. 2012, 11: 25-2840. 10.1186/1475-2840-11-25. 11-25PubMedCentralCrossRefPubMed Den Engelsen C, Koekkoek PS, Gorter KJ, Van den Donk M, Salome PL, Rutten GE: High-sensitivity C-reactive protein to detect metabolic syndrome in a centrally obese population: a cross-sectional analysis. Cardiovasc Diabetol. 2012, 11: 25-2840. 10.1186/1475-2840-11-25. 11-25PubMedCentralCrossRefPubMed
27.
go back to reference Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC, Spertus JA, Costa F: American Heart Association, National Heart, Lung, and Blood Institute: Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005, 112 (17): 2735-2752. 10.1161/CIRCULATIONAHA.105.169404.CrossRefPubMed Grundy SM, Cleeman JI, Daniels SR, Donato KA, Eckel RH, Franklin BA, Gordon DJ, Krauss RM, Savage PJ, Smith SC, Spertus JA, Costa F: American Heart Association, National Heart, Lung, and Blood Institute: Diagnosis and management of the metabolic syndrome: an American Heart Association/National Heart, Lung, and Blood Institute Scientific Statement. Circulation. 2005, 112 (17): 2735-2752. 10.1161/CIRCULATIONAHA.105.169404.CrossRefPubMed
28.
go back to reference Tisdale WA, Klatskin G, Kinsella ED: The significance of the direct-reacting fraction of serum Bilirubin in hemolytic jaundice. Am J Med. 1959, 26 (2): 214-227. 10.1016/0002-9343(59)90310-9.CrossRefPubMed Tisdale WA, Klatskin G, Kinsella ED: The significance of the direct-reacting fraction of serum Bilirubin in hemolytic jaundice. Am J Med. 1959, 26 (2): 214-227. 10.1016/0002-9343(59)90310-9.CrossRefPubMed
29.
go back to reference Zelle DM, Deetman N, Alkhalaf A, Navis G, Bakker SJ: Support for a protective effect of Bilirubin on diabetic nephropathy in humans. Kidney Int. 2011, 79 (6): 686-7.CrossRefPubMed Zelle DM, Deetman N, Alkhalaf A, Navis G, Bakker SJ: Support for a protective effect of Bilirubin on diabetic nephropathy in humans. Kidney Int. 2011, 79 (6): 686-7.CrossRefPubMed
30.
go back to reference Katsiki N, Karagiannis A, Mikhailidis DP: Diabetes, bilirubin and amputations: is there a link?. Diabetologia. 2013, 56 (4): 683-685. 10.1007/s00125-013-2840-1.CrossRefPubMed Katsiki N, Karagiannis A, Mikhailidis DP: Diabetes, bilirubin and amputations: is there a link?. Diabetologia. 2013, 56 (4): 683-685. 10.1007/s00125-013-2840-1.CrossRefPubMed
31.
go back to reference Deetman PE, Zelle DM, Van der Heide JJ H, Navis GJ, Gans RO, Bakker SJ: Plasma bilirubin and late graft failure in renal transplant recipients. Transpl Int. 2012, 25 (8): 876-881. 10.1111/j.1432-2277.2012.01515.x.CrossRefPubMed Deetman PE, Zelle DM, Van der Heide JJ H, Navis GJ, Gans RO, Bakker SJ: Plasma bilirubin and late graft failure in renal transplant recipients. Transpl Int. 2012, 25 (8): 876-881. 10.1111/j.1432-2277.2012.01515.x.CrossRefPubMed
32.
go back to reference Hazenberg BP, Limburg PC, Bijzet J, Van Rijswijk MH: A quantitative method for detecting deposits of amyloid A protein in aspirated fat tissue of patients with arthritis. Ann Rheum Dis. 1999, 58 (2): 96-102. 10.1136/ard.58.2.96.PubMedCentralCrossRefPubMed Hazenberg BP, Limburg PC, Bijzet J, Van Rijswijk MH: A quantitative method for detecting deposits of amyloid A protein in aspirated fat tissue of patients with arthritis. Ann Rheum Dis. 1999, 58 (2): 96-102. 10.1136/ard.58.2.96.PubMedCentralCrossRefPubMed
33.
go back to reference Selvin S: Statistical Analysis of Epidemiological Data. 1996, New York: Oxford University Press Selvin S: Statistical Analysis of Epidemiological Data. 1996, New York: Oxford University Press
34.
go back to reference Lu M, Lyden PD, Brott TG, Hamilton S, Broderick JP, Grotta JC: Beyond subgroup analysis: improving the clinical interpretation of treatment effects in stroke research. J Neurosci Methods. 2005, 143 (2): 209-216. 10.1016/j.jneumeth.2004.10.002.CrossRefPubMed Lu M, Lyden PD, Brott TG, Hamilton S, Broderick JP, Grotta JC: Beyond subgroup analysis: improving the clinical interpretation of treatment effects in stroke research. J Neurosci Methods. 2005, 143 (2): 209-216. 10.1016/j.jneumeth.2004.10.002.CrossRefPubMed
35.
go back to reference Jenko-Praznikar Z, Petelin A, Jurdana M, Ziberna L: Serum bilirubin levels are lower in overweight asymptomatic middle-aged adults: An early indicator of metabolic syndrome?. Metabolism. 2013, 62 (7): 976-985. 10.1016/j.metabol.2013.01.011.CrossRefPubMed Jenko-Praznikar Z, Petelin A, Jurdana M, Ziberna L: Serum bilirubin levels are lower in overweight asymptomatic middle-aged adults: An early indicator of metabolic syndrome?. Metabolism. 2013, 62 (7): 976-985. 10.1016/j.metabol.2013.01.011.CrossRefPubMed
36.
go back to reference Lin LY, Kuo HK, Hwang JJ, Lai LP, Chiang FT, Tseng CD, Lin JL: Serum bilirubin is inversely associated with insulin resistance and metabolic syndrome among children and adolescents. Atherosclerosis. 2009, 203 (2): 563-568. 10.1016/j.atherosclerosis.2008.07.021.CrossRefPubMed Lin LY, Kuo HK, Hwang JJ, Lai LP, Chiang FT, Tseng CD, Lin JL: Serum bilirubin is inversely associated with insulin resistance and metabolic syndrome among children and adolescents. Atherosclerosis. 2009, 203 (2): 563-568. 10.1016/j.atherosclerosis.2008.07.021.CrossRefPubMed
37.
go back to reference Ohnaka K, Kono S, Inoguchi T, Yin G, Morita M, Adachi M, Kawate H, Takayanagi R: Inverse associations of serum bilirubin with high sensitivity C-reactive protein, glycated hemoglobin, and prevalence of type 2 diabetes in middle-aged and elderly Japanese men and women. Diabetes Res Clin Pract. 2010, 88 (1): 103-110. 10.1016/j.diabres.2009.12.022.CrossRefPubMed Ohnaka K, Kono S, Inoguchi T, Yin G, Morita M, Adachi M, Kawate H, Takayanagi R: Inverse associations of serum bilirubin with high sensitivity C-reactive protein, glycated hemoglobin, and prevalence of type 2 diabetes in middle-aged and elderly Japanese men and women. Diabetes Res Clin Pract. 2010, 88 (1): 103-110. 10.1016/j.diabres.2009.12.022.CrossRefPubMed
38.
go back to reference Basiglio CL, Arriaga SM, Pelusa F, Almara AM, Kapitulnik J, Mottino AD: Complement activation and disease: protective effects of hyperbilirubinaemia. Clin Sci (Lond). 2009, 118 (2): 99-113. 10.1042/CS20080540.CrossRef Basiglio CL, Arriaga SM, Pelusa F, Almara AM, Kapitulnik J, Mottino AD: Complement activation and disease: protective effects of hyperbilirubinaemia. Clin Sci (Lond). 2009, 118 (2): 99-113. 10.1042/CS20080540.CrossRef
39.
go back to reference Rocuts F, Zhang X, Yan J, Yue Y, Thomas M, Bach FH, Czismadia E, Wang H: Bilirubin promotes de novo generation of T regulatory cells. Cell Transplant. 2010, 19 (4): 443-451. 10.3727/096368909X484680.CrossRefPubMed Rocuts F, Zhang X, Yan J, Yue Y, Thomas M, Bach FH, Czismadia E, Wang H: Bilirubin promotes de novo generation of T regulatory cells. Cell Transplant. 2010, 19 (4): 443-451. 10.3727/096368909X484680.CrossRefPubMed
40.
go back to reference Rutter MK, Meigs JB, Sullivan LM, D’Agostino RBS, Wilson PW: C-reactive protein, the metabolic syndrome, and prediction of cardiovascular events in the Framingham Offspring Study. Circulation. 2004, 110 (4): 380-385. 10.1161/01.CIR.0000136581.59584.0E.CrossRefPubMed Rutter MK, Meigs JB, Sullivan LM, D’Agostino RBS, Wilson PW: C-reactive protein, the metabolic syndrome, and prediction of cardiovascular events in the Framingham Offspring Study. Circulation. 2004, 110 (4): 380-385. 10.1161/01.CIR.0000136581.59584.0E.CrossRefPubMed
41.
go back to reference Garin MC, Kalix B, Morabia A, James RW: Small, dense lipoprotein particles and reduced paraoxonase-1 in patients with the metabolic syndrome. J Clin Endocrinol Metab. 2005, 90 (4): 2264-2269. 10.1210/jc.2004-1295.CrossRefPubMed Garin MC, Kalix B, Morabia A, James RW: Small, dense lipoprotein particles and reduced paraoxonase-1 in patients with the metabolic syndrome. J Clin Endocrinol Metab. 2005, 90 (4): 2264-2269. 10.1210/jc.2004-1295.CrossRefPubMed
42.
go back to reference Dullaart RP, Kwakernaak AJ, Dallinga-Thie GM: The positive relationship of serum paraoxonase-1 activity with apolipoprotein E is abrogated in metabolic syndrome. Atherosclerosis. 2013, 230 (1): 6-11. 10.1016/j.atherosclerosis.2013.06.019.CrossRefPubMed Dullaart RP, Kwakernaak AJ, Dallinga-Thie GM: The positive relationship of serum paraoxonase-1 activity with apolipoprotein E is abrogated in metabolic syndrome. Atherosclerosis. 2013, 230 (1): 6-11. 10.1016/j.atherosclerosis.2013.06.019.CrossRefPubMed
Metadata
Title
High sensitive C-reactive protein and serum amyloid A are inversely related to serum bilirubin: effect-modification by metabolic syndrome
Authors
Petronella E Deetman
Stephan JL Bakker
Robin PF Dullaart
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Cardiovascular Diabetology / Issue 1/2013
Electronic ISSN: 1475-2840
DOI
https://doi.org/10.1186/1475-2840-12-166

Other articles of this Issue 1/2013

Cardiovascular Diabetology 1/2013 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