DOI QR코드

DOI QR Code

ApoB/ApoA-I ratio is independently associated with carotid atherosclerosis in type 2 diabetes mellitus with well-controlled LDL cholesterol levels

  • Jun, Ji Eun (Division of Endocrinology and Metabolism, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Choi, Young Ju (Huh's Diabetes Center and 21st Century Diabetes and Vascular Research Institute) ;
  • Lee, Yong-Ho (Division of Endocrinology and Metabolism, Department of Internal Medicine, Yonsei University College of Medicine) ;
  • Kim, Dae Jung (Department of Endocrinology and Metabolism, Ajou University School of Medicine) ;
  • Park, Seok Won (Department of Internal Medicine, CHA University) ;
  • Huh, Byung Wook (Huh's Diabetes Center and 21st Century Diabetes and Vascular Research Institute) ;
  • Lee, Eun Jig (Division of Endocrinology and Metabolism, Department of Internal Medicine, Yonsei University College of Medicine) ;
  • Jee, Sun-Ha (Department of Epidemiology and Health Promotion, Institute for Health Promotion, Yonsei University Graduate School of Public Health) ;
  • Hur, Kyu Yeon (Division of Endocrinology and Metabolism, Department of Medicine, Samsung Medical Center, Sungkyunkwan University School of Medicine) ;
  • Choi, Sung Hee (Department of Internal Medicine, Seoul National University Bundang Hospital) ;
  • Huh, Kap Bum (Huh's Diabetes Center and 21st Century Diabetes and Vascular Research Institute)
  • 투고 : 2017.11.28
  • 심사 : 2017.12.12
  • 발행 : 2018.01.01

초록

Background/Aims: This study aimed to investigate whether the apolipoprotein (Apo) B/ApoA-I ratio is associated with carotid intima-media thickness (CIMT) in type 2 diabetes mellitus (T2DM) subjects with low density lipoprotein cholesterol (LDL-C) levels less than 100 mg/dL. Methods: This cross-sectional study included 845 subjects aged with T2DM 40 to 75 years who had visited Huh's Diabetes Center in Seoul, Republic of Korea for CIMT measurement. Traditional fasting lipid profiles, ApoB and ApoA-I levels were examined. CIMT was measured at three points on the far wall of 1 cm long section of the common carotid artery in the proximity of the carotid bulb. The mean value of six measurements from right and left carotid arteries were used as the mean CIMT. In this study, carotid atherosclerosis was defined as having a focal plaque or diffuse thickening of the carotid wall (mean CIMT ${\geq}1.0mm$) Results: The prevalence of carotid atherosclerosis increased with ApoB/ApoA-I ratio. The ApoB/ApoA-I ratio, expressed as both quartiles (odds ratio [OR], 2.14; 95% confidence interval [CI], 1.21 to 3.79; p for trend = 0.014) and continuous values (OR, 10.05; 95% CI, 3.26 to 30.97; p < 0.001), was significantly associated with a higher risk for carotid atherosclerosis, regardless of conventional cardiovascular disease risk factors. The optimal ApoB/ApoA-I ratio cutoff value for detecting carotid atherosclerosis was 0.57, based on receiver operating characteristic curve analysis with a sensitivity of 58.0% and a specificity of 55.1%. Conclusions: A high ApoB/ApoA-I ratio was significantly associated with carotid atherosclerosis in T2DM patients with LDL-C levels less than 100 mg/dL.

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참고문헌

  1. American Diabetes Association. 9. Cardiovascular disease and risk management. Diabetes Care 2017;40(Suppl 1):S75-S87. https://doi.org/10.2337/dc17-S012
  2. Stone NJ, Robinson JG, Lichtenstein AH, et al. 2013 ACC/AHA guideline on the treatment of blood cholesterol to reduce atherosclerotic cardiovascular risk in adults: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2014;63(25 Pt B):2889-2934. https://doi.org/10.1016/j.jacc.2013.11.002
  3. Expert Dyslipidemia Panel of the International Atherosclerosis Society Panel members. An International Atherosclerosis Society Position Paper: global recommendations for the management of dyslipidemia: full report. J Clin Lipidol 2014;8:29-60. https://doi.org/10.1016/j.jacl.2013.12.005
  4. Ha KH, Kim DJ. Current status of managing diabetes mellitus in Korea. Korean J Intern Med 2016;31:845-850. https://doi.org/10.3904/kjim.2016.253
  5. Ai M, Otokozawa S, Asztalos BF, et al. Small dense LDL cholesterol and coronary heart disease: results from the Framingham Offspring Study. Clin Chem 2010;56:967-976. https://doi.org/10.1373/clinchem.2009.137489
  6. Lim TS, Yun JS, Cha SA, et al. Elevated lipoprotein(a) levels predict cardiovascular disease in type 2 diabetes mellitus: a 10-year prospective cohort study. Korean J Intern Med 2016;31:1110-1119. https://doi.org/10.3904/kjim.2016.030
  7. Ivanova EA, Myasoedova VA, Melnichenko AA, Grechko AV, Orekhov AN. Small dense low-density lipoprotein as biomarker for atherosclerotic diseases. Oxid Med Cell Longev 2017;2017:1273042.
  8. Cromwell WC, Otvos JD. Heterogeneity of low-density lipoprotein particle number in patients with type 2 diabetes mellitus and low-density lipoprotein cholesterol <100 mg/dl. Am J Cardiol 2006;98:1599-1602. https://doi.org/10.1016/j.amjcard.2006.07.036
  9. Walldius G, Jungner I. The apoB/apoA-I ratio: a strong, new risk factor for cardiovascular disease and a target for lipid-lowering therapy: a review of the evidence. J Intern Med 2006;259:493-519. https://doi.org/10.1111/j.1365-2796.2006.01643.x
  10. Kaneva AM, Potolitsyna NN, Bojko ER, Odland JO. The apolipoprotein B/apolipoprotein A-I ratio as a potential marker of plasma atherogenicity. Dis Markers 2015;2015:591454.
  11. Millan J, Pinto X, Munoz A, et al. Lipoprotein ratios: physiological significance and clinical usefulness in cardiovascular prevention. Vasc Health Risk Manag 2009;5:757-765.
  12. Yusuf S, Hawken S, Ounpuu S, et al. Effect of potentially modifiable risk factors associated with myocardial infarction in 52 countries (the INTERHEART study): case-control study. Lancet 2004;364:937-952. https://doi.org/10.1016/S0140-6736(04)17018-9
  13. Meisinger C, Loewel H, Mraz W, Koenig W. Prognostic value of apolipoprotein B and A-I in the prediction of myocardial infarction in middle-aged men and women: results from the MONICA/KORA Augsburg cohort study. Eur Heart J 2005;26:271-278. https://doi.org/10.1093/eurheartj/ehi003
  14. Walldius G, Jungner I, Holme I, Aastveit AH, Kolar W, Steiner E. High apolipoprotein B, low apolipoprotein A-I, and improvement in the prediction of fatal myocardial infarction (AMORIS study): a prospective study. Lancet 2001;358:2026-2033. https://doi.org/10.1016/S0140-6736(01)07098-2
  15. Walldius G, Jungner I, Aastveit AH, Holme I, Furberg CD, Sniderman AD. The apoB/apoA-I ratio is better than the cholesterol ratios to estimate the balance between plasma proatherogenic and antiatherogenic lipoproteins and to predict coronary risk. Clin Chem Lab Med 2004;42:1355-1363.
  16. Verges B. Pathophysiology of diabetic dyslipidaemia: where are we? Diabetologia 2015;58:886-899. https://doi.org/10.1007/s00125-015-3525-8
  17. Kannan S, Mahadevan S, Ramji B, Jayapaul M, Kumaravel V. LDL-cholesterol: Friedewald calculated versus direct measurement-study from a large Indian laboratory database. Indian J Endocrinol Metab 2014;18:502-504. https://doi.org/10.4103/2230-8210.137496
  18. Bonora E, Moghetti P, Zancanaro C, et al. Estimates of in vivo insulin action in man: comparison of insulin tolerance tests with euglycemic and hyperglycemic glucose clamp studies. J Clin Endocrinol Metab 1989;68:374-378. https://doi.org/10.1210/jcem-68-2-374
  19. Young RP, Critchley JA, Anderson PJ, Lau MS, Lee KK, Chan JC. The short insulin tolerance test: feasibility study using venous sampling. Diabet Med 1996;13:429-433. https://doi.org/10.1002/(SICI)1096-9136(199605)13:5<429::AID-DIA98>3.0.CO;2-K
  20. Alberti KG, Daly ME, Robinson A, Marshall SM, Mathers JC. The short insulin tolerance test is safe and reproducible. Diabet Med 1999;16:352-353. https://doi.org/10.1046/j.1464-5491.1999.00048.x
  21. Park SW, Kim SK, Cho YW, et al. Insulin resistance and carotid atherosclerosis in patients with type 2 diabetes. Atherosclerosis 2009;205:309-313. https://doi.org/10.1016/j.atherosclerosis.2008.12.006
  22. Chambless LE, Folsom AR, Clegg LX, et al. Carotid wall thickness is predictive of incident clinical stroke: the Atherosclerosis Risk in Communities (ARIC) study. Am J Epidemiol 2000;151:478-487. https://doi.org/10.1093/oxfordjournals.aje.a010233
  23. Hong SN, Park JC, Yoon NS, et al. Carotid artery intima-media thickness in Behcet's disease patients without significant cardiovascular involvement. Korean J Intern Med 2008;23:87-93. https://doi.org/10.3904/kjim.2008.23.2.87
  24. Baldassarre D, Amato M, Pustina L, et al. Measurement of carotid artery intima-media thickness in dyslipidemic patients increases the power of traditional risk factors to predict cardiovascular events. Atherosclerosis 2007;191:403-408. https://doi.org/10.1016/j.atherosclerosis.2006.04.008
  25. Naqvi TZ, Lee MS. Carotid intima-media thickness and plaque in cardiovascular risk assessment. JACC Cardiovasc Imaging 2014;7:1025-1038. https://doi.org/10.1016/j.jcmg.2013.11.014
  26. Touboul PJ, Hennerici MG, Meairs S, et al. Mannheim carotid intima-media thickness and plaque consensus (2004-2006-2011). An update on behalf of the advisory board of the 3rd, 4th and 5th watching the risk symposia, at the 13th, 15th and 20th European Stroke Conferences, Mannheim, Germany, 2004, Brussels, Belgium, 2006, and Hamburg, Germany, 2011. Cerebrovasc Dis 2012;34:290-296. https://doi.org/10.1159/000343145
  27. Kim SK, Choi YJ, Huh BW, et al. Ratio of waist-to-calf circumference and carotid atherosclerosis in Korean patients with type 2 diabetes. Diabetes Care 2011;34:2067-2071. https://doi.org/10.2337/dc11-0743
  28. Packard CJ, Shepherd J. Lipoprotein heterogeneity and apolipoprotein B metabolism. Arterioscler Thromb Vasc Biol 1997;17:3542-3556. https://doi.org/10.1161/01.ATV.17.12.3542
  29. Walldius G, Jungner I. Apolipoprotein B and apolipoprotein A-I: risk indicators of coronary heart disease and targets for lipid-modifying therapy. J Intern Med 2004;255:188-205. https://doi.org/10.1046/j.1365-2796.2003.01276.x
  30. McQueen MJ, Hawken S, Wang X, et al. Lipids, lipoproteins, and apolipoproteins as risk markers of myocardial infarction in 52 countries (the INTERHEART study): a case-control study. Lancet 2008;372:224-233. https://doi.org/10.1016/S0140-6736(08)61076-4
  31. Canoui-Poitrine F, Luc G, Bard JM, et al. Relative contribution of lipids and apolipoproteins to incident coronary heart disease and ischemic stroke: the PRIME Study. Cerebrovasc Dis 2010;30:252-259. https://doi.org/10.1159/000319067
  32. Thompson A, Danesh J. Associations between apolipoprotein B, apolipoprotein AI, the apolipoprotein B/AI ratio and coronary heart disease: a literature-based meta-analysis of prospective studies. J Intern Med 2006;259:481-492. https://doi.org/10.1111/j.1365-2796.2006.01644.x
  33. Jadhav UM, Kadam NN. Apolipoproteins: correlation with carotid intimamedia thickness and coronary artery disease. J Assoc Physicians India 2004;52:370-375.
  34. Jung CH, Hwang JY, Shin MS, et al. Association of apolipoprotein b/apolipoprotein A1 ratio and coronary artery stenosis and plaques detected by multi-detector computed tomography in healthy population. J Korean Med Sci 2013;28:709-716. https://doi.org/10.3346/jkms.2013.28.5.709
  35. Wallenfeldt K, Bokemark L, Wikstrand J, Hulthe J, Fagerberg B. Apolipoprotein B/apolipoprotein A-I in relation to the metabolic syndrome and change in carotid artery intima-media thickness during 3 years in middle-aged men. Stroke 2004;35:2248-2252. https://doi.org/10.1161/01.STR.0000140629.65145.3c
  36. Goldberg IJ. Clinical review 124: diabetic dyslipidemia: causes and consequences. J Clin Endocrinol Metab 2001;86:965-971. https://doi.org/10.1210/jcem.86.3.7304
  37. Haffner SM, Mykkanen L, Festa A, Burke JP, Stern MP. Insulin-resistant prediabetic subjects have more atherogenic risk factors than insulin-sensitive prediabetic subjects: implications for preventing coronary heart disease during the prediabetic state. Circulation 2000;101:975-980. https://doi.org/10.1161/01.CIR.101.9.975
  38. Sniderman AD, Faraj M. Apolipoprotein B, apolipoprotein A-I, insulin resistance and the metabolic syndrome. Curr Opin Lipidol 2007;18:633-637. https://doi.org/10.1097/MOL.0b013e3282f0dd33
  39. Bruno G, Merletti F, Biggeri A, et al. Effect of age on the association of non-high-density-lipoprotein cholesterol and apolipoprotein B with cardiovascular mortality in a Mediterranean population with type 2 diabetes: the Casale Monferrato study. Diabetologia 2006;49:937-944. https://doi.org/10.1007/s00125-006-0195-6
  40. Dahlen EM, Lanne T, Engvall J, et al. Carotid intima-media thickness and apolipoprotein B/apolipoprotein A-I ratio in middle-aged patients with type 2 diabetes. Diabet Med 2009;26:384-390. https://doi.org/10.1111/j.1464-5491.2009.02693.x
  41. Anagnostis P, Stevenson JC, Crook D, Johnston DG, Godsland IF. Effects of menopause, gender and age on lipids and high-density lipoprotein cholesterol subfractions. Maturitas 2015;81:62-68. https://doi.org/10.1016/j.maturitas.2015.02.262
  42. Goff DC Jr, Lloyd-Jones DM, Bennett G, et al. 2013 ACC/AHA guideline on the assessment of cardiovascular risk: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines. Circulation 2014;129(25 Suppl 2):S49-S73. https://doi.org/10.1161/01.cir.0000437741.48606.98
  43. NACB LMPG Committee Members, Myers GL, Christenson RH, et al. National Academy of Clinical Biochemistry Laboratory Medicine Practice guidelines: emerging biomarkers for primary prevention of cardiovascular disease. Clin Chem 2009;55:378-384.

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