Plasma total bilirubin levels predict amputation events in type 2 diabetes mellitus: The Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) study

Diabetologia

Volumn 56, Issue 4, 2013, Pages 724-736

  Chan, K H ^a,b,c,d   O'Connell, R L ^d   Sullivan, D R ^a,d   Hoffmann, L S ^d   Rajamani, K ^a,d   Whiting, M ^e   Donoghoe, M W ^d   Vanhala, M ^f   Hamer, A ^g   Yu, B ^a,b   Stocker, R ^d   Ng, M K C ^a,b,c   Keech, A C ^a,b,d  

^a ROYAL PRINCE ALFRED HOSPITAL   (Australia)

^b UNIVERSITY OF SYDNEY   (Australia)

^c HEART RESEARCH INSTITUTE   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e FLINDERS MEDICAL CENTRE   (Australia)

^f Central Finland Central Hospital   (Finland)

^g NELSON HOSPITAL   (New Zealand)

Author keywords

Amputation; Bilirubin; Fenofibrate Intervention and Event Lowering in Diabetes (FIELD) study; Peripheral arterial disease; Type 2 diabetes mellitus

Indexed keywords

BILIRUBIN; FENOFIBRATE; GAMMA GLUTAMYLTRANSFERASE; HEMOGLOBIN A1C; PLACEBO;

ADULT; AGE; AGED; ARTICLE; BILIRUBIN BLOOD LEVEL; BODY HEIGHT; CARDIOVASCULAR DISEASE; COHORT ANALYSIS; CONTROLLED STUDY; DIABETIC FOOT; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; FEMALE; GAMMA GLUTAMYL TRANSFERASE BLOOD LEVEL; HIGH RISK POPULATION; HUMAN; LEG AMPUTATION; LONGITUDINAL STUDY; MAJOR CLINICAL STUDY; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PERIPHERAL OCCLUSIVE ARTERY DISEASE; PREDICTION; PRIORITY JOURNAL; SMOKING;

AGED; AMPUTATION; ANTIOXIDANTS; BILIRUBIN; BIOLOGICAL MARKERS; COHORT STUDIES; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 2; FEMALE; FENOFIBRATE; HUMANS; LOWER EXTREMITY; MALE; MIDDLE AGED; PREDICTIVE VALUE OF TESTS; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RISK FACTORS; SEX FACTORS; TREATMENT OUTCOME;

EID: 84876495389     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-012-2818-4     Document Type: Article

References (50)

1. Gordois A, Scuffham P, Shearer A (2003) The health care cost of diabetic peripheral neuropathy in the US. Diabetes Care 26:1790-1795
2. Tongers J, Roncalli J, Losordo D (2008) Therapeutic angiogenesis for critical limb ischemia: microvascular therapies coming of age. Circulation 118:9-16
3. Rajamani K, Colman P, Li L et al (2009) Effect of fenofibrate on amputation events in people with type 2 diabetes mellitus (FIELD study): a prespecified analysis of a randomised controlled trial. Lancet 373:1780-1788
4. Ohnaka K, Kono S (2010) Bilirubin, cardiovascular diseases and cancer: epidemiological perspectives. Expert Rev Endocrinol Metab 5:891-904
5. Breimer L, Mikhailidis D (2011) Is bilirubin a marker of vascular disease and/or cancer and is it a potential therapeutic target? Curr Pharm Des 17:3644-3655
6. Lin J, Vitek L, Schwertner H (2010) Serum bilirubin and genes controlling bilirubin concentrations as biomarkers for cardiovascular disease. Clin Chem 56:1535-1543
7. Stocker R, Perrella M (2006) Heme oxygenase-1: a novel drug target for atherosclerotic diseases? Circulation 114:2178-2189
8. Chan K, Ng M, Stocker R (2011) Haem oxygenase-1 and cardiovascular disease: mechanisms and therapeutic potential. Clin Sci (Lond) 120:493-504
9. Kawamura K, Ishikawa K, Wada Y et al (2005) Bilirubin from heme oxygenase-1 attenuates vascular endothelial activation and dysfunction. Arterioscler Thromb Vasc Biol 25:155-160
10. Stocker R, Yamamoto Y, McDonagh A, Glazer A, Ames B (1987) Bilirubin is an antioxidant of possible physiological importance. Science 235:1043-1046
11. Stocker R, Glazer A, Ames B (1987) Antioxidant activity of albumin-bound bilirubin. Proc Natl Acad Sci USA 84:5918-5922
12. Inoguchi T, Sasaki S, Kobayashi K, Takayanagi R, Yamada T (2007) Relationship between Gilbert Syndrome and prevalence of vascular complications in patients with diabetes. JAMA 12:1398-1400
13. Tapan S, Dogru T, Tasci I, Ercin C, Ozgurtas T, Erbil M (2009) Soluble CD40 ligand and soluble P-selectin levels in Gilbert's syndrome: a link to protection against atherosclerosis? Clin Biochem 42:791-795
14. VItek L, Jirsa M, Brodanova M et al (2002) Gilbert syndrome and ischemic heart disease: a protective effect of elevated bilirubin levels. Atherosclerosis 160:449-456
15. Abraham N, Kappas A (2008) Pharmacological and clinical aspects of heme oxygenase. Pharmacol Rev 60:79-127
16. Stocker R, Keaney JF (2004) Role of oxidative modifications in atherosclerosis. Physiol Rev 84:1381-1478
17. Breimer L, Spyropolous K, Winder A, Mikhailidis D, Hamilton G (1994) Is bilirubin protective against coronary artery disease? Clin Chem 40:1987-1988
18. Rantner B, Kollerits B, Anderwald-Stadler M et al (2008) Association between the UGT1A1 TA-repeat polymorphism and bilirubin concentration in patients with intermittent claudication: results from the CAVASIC study. Clin Chem 54:851-857
19. Perlstein T, Pande R, Beckman J, Creager M (2008) Serum total bilirubin level and prevalent lower-extremity peripheral arterial disease: National Health and Nutrition Examination Survey (NHANES) 1999 to 2004. Arterioscler Thromb Vasc Biol 28:166-172
20. Wang H, Han P, Zhang W et al (2012) Serum bilirubin level is negatively correlated with disease progression of peripheral arterial disease: an observational cohort study. Angiology 63:248-253
21. Johannesson A, Larsson G, Ramstrand N, Turkiewicz A, Wiréhn A, Atroshi I (2009) Incidence of lower-limb amputation in the diabetic and nondiabetic general population: a 10-year population-based cohort study of initial unilateral and contralateral amputations and reamputations. Diabetes Care 32:275-280
22. The FIELD Study Investigators (2005) Effects of long-term fenofibrate therapy on cardiovascular events in 9795 people with type 2 diabetes mellitus (the FIELD study): randomised controlled trial. Lancet 366:1849-1861
23. Barrett-Connor E, Orchard T (1985) Diabetes and heart disease. In: National Diabetes Data Group. Diabetes in America: diabetes data compiled 1984. US Department of Health and Human Services, Washington, pp XVI, 1-41
24. Nakayama K (1995) Differences between enzymatic and diazo methods for measuring direct bilirubin. Eur J Clin Chem Clin Biochem 33:513-517
25. Selvin E, Erlinger T (2004) Prevalence of and risk factors for peripheral arterial disease in the United States: results from the National Health and Nutrition Examination Survey, 1999-2000. Circulation 110:738-743
26. Pasta D (2009) Learning when to be discrete: continuous vs. categorical predictors. SAS Glob Forum Pap 248:1-10
27. Djousse L, Levy D, Cupples L, Evans J, D'Agostino R, Ellison R (2001) Total serum bilirubin and risk of cardiovascular disease in the Framingham offspring study. Am J Cardiol 87:1196-1200
28. Ekblom K, Marklund S, Jansson J et al (2010) Plasma bilirubin and UGT1A128 are not protective factors against first-time myocardial infarction in a prospective, nested case-referent setting. Circ Cardiovasc Genet 3:340-347
29. Schwertner H, Jackson W, Tolan G (1994) Association of low serum concentration of bilirubin with increased risk of coronary artery disease. Clin Chem 40:18-23
30. Breimer L, Wannamethee G, Ebrahim S, Shaper A (1995) Serum bilirubin and risk of ischemic heart disease in middle-aged British men. Clin Chem 41:1504-1508
31. Hopkins P, Wu L, Hunt S, James B, Vincent M, Wiliams R (1996) Higher serum bilirubin is associated with decreased risk for early familial coronary artery disease. Arterioscler Thromb Vasc Biol 16:250-255
32. Madhavan M, Wattigney W, Srinivasan S, Berenson G (1997) Serum bilirubin distribution and its relation to cardiovascular risk in children and young adults. Atherosclerosis 131:107-113
33. Temme E, Zhang J, Schouten E, Kesteloot H (2001) Serum bilirubin and 10-year mortality risk in a Belgian population. Cancer Causes Control 12:887-894
34. Bosma P, van der Meer IM, Bakker C, Hofman A, Paul-Abrahamse M, Witteman J (2003) UGT1A128 allele and coronary heart disease: the Rotterdam Study. Clin Chem 49:1180-1181
35. Novotny L, VItek L (2003) Inverse relationship between serum bilirubin and atherosclerosis in men. A meta-analysis of published studies. Exp Biol Med 228:568-571
36. Lin J, O'Donnell C, Schwaiger J et al (2006) Association between the UGT1A128 allele, bilirubin levels, and coronary heart disease. Circulation 114:1476-1481
37. Troughton J, Woodside J, Young I et al (2007) Bilirubin and coronary heart disease risk in the Prospective Epidemiological Study of Myocardial Infarction (PRIME). Eur J Cardiovasc Prev Rehabil 14:79-84
38. Chen Y, Chau L, Chen J, Lin S (2008) Serum bilirubin and ferritin levels link heme oxygenase-1 gene promoter polymorphism and susceptibility to coronary artery disease in diabetic patients. Diabetes Care 31:1615-1620
39. Kimm H, Yun J, Jo J, Jee S (2009) Low serum bilirubin level as an independent predictor of stroke incidence: a prospective study in Korean men and women. Stroke 40:3422-3427
40. Erdogan D, Gullu H, Yildirim E et al (2006) Low serum bilirubin levels are independently and inversely related to impaired flow-mediated vasodilation and increased carotid intima-media thickness in both men and women. Atherosclerosis 184:431-437
41. Vítek L, Novotny L, Sperl M, Holaj R, Spacil J (2006) The inverse association of elevated serum bilirubin levels with subclinical carotid atherosclerosis. Cerebrovasc Dis 21:408-414
42. Maruhashi T, Soga J, Fujimura N et al (2012) Hyperbilirubinemia, augmentation of endothelial function, and decrease in oxidative stress in Gilbert syndrome. Circulation 126:598-603
43. Öllinger R, Bilban M, Erat A et al (2005) Bilirubin: a natural inhibitor of vascular smooth muscle cell proliferation. Circulation 112:1030-1039
44. Tenhunen R, Marver H, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61:748-755
45. Endler G, Exner M, Schillinger M et al (2004) A microsatellite polymorphism in the heme oxygenase-1 gene promoter is associated with increased bilirubin and HDL levels but not with coronary artery disease. Thromb Haemost 91:155-161
46. Lublinghoff N, Winkler K, Winkelmann B et al (2009) Genetic variants of the promoter of the heme oxygenase-1 gene and their influence on cardiovascular disease (the Ludwigshafen Risk and Cardiovascular Health study). BMC Med Genet 10:36
47. Gajdos V, Petit F, Perret C et al (2006) Further evidence that the UGT1A128 allele is not associated with coronary heart disease: the ECTIM Study. Clin Chem 52:2313-2314
48. Oda E (2010) Bilirubin is negatively associated with A1C independently of fasting plasma glucose, age, obesity, inflammation, hemoglobin, and iron in apparently healthy Japanese men and women. Diabetes Care 22:e131
49. Ohnaka K, Kono S, Inoguchi T et al (2010) 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 88:103-110
50. Ames B, Cathcart R, Schwiers E, Hochstein P (1981) Uric acid provides an antioxidant defense in humans against oxidant- and radical-caused aging and cancer: a hypothesis. Proc Natl Acad Sci U S A 78:6858-6862