DOI QR코드

DOI QR Code

Diabetes and Subclinical Coronary Atherosclerosis

  • Lee, Chang Hoon (Department of Cardiology, Veterans Health Service Medical Center) ;
  • Lee, Seung-Whan (Department of Cardiology, Asan Medical Center, University of Ulsan College of Medicine) ;
  • Park, Seong-Wook (Department of Cardiology, Asan Medical Center, University of Ulsan College of Medicine)
  • Received : 2018.03.06
  • Accepted : 2018.08.20
  • Published : 2018.10.17

Abstract

It is well known that diabetic patients have a high risk of cardiovascular events, and although there has been a tremendous effort to reduce these cardiovascular risks, the incidence of cardiovascular morbidity and mortality in diabetic patients remains high. Therefore, the early detection of coronary artery disease (CAD) is necessary in those diabetic patients who are at risk of cardiovascular events. Significant medical and radiological advancements, including coronary computed tomography angiography (CCTA), mean that it is now possible to investigate the characteristics of plaques, instead of solely evaluating the calcium level of the coronary artery. Recently, several studies reported that the prevalence of subclinical coronary atherosclerosis (SCA) is higher than expected, and this could impact on CAD progression in asymptomatic diabetic patients. In addition, several reports suggest the potential benefit of using CCTA for screening for SCA in asymptomatic diabetic patients, which might dramatically decrease the incidence of cardiovascular events. For these reasons, the medical interest in SCA in diabetic patients is increasing. In this article, we sought to review the results of studies on CAD in asymptomatic diabetic patients and discuss the clinical significance and possibility of using CCTA to screen for SCA.

Keywords

References

  1. Gregg EW, Gu Q, Cheng YJ, Narayan KM, Cowie CC. Mortality trends in men and women with diabetes, 1971 to 2000. Ann Intern Med 2007;147:149-55. https://doi.org/10.7326/0003-4819-147-3-200708070-00167
  2. Bax JJ, Inzucchi SE, Bonow RO, Schuijf JD, Freeman MR, Barrett EJ; Global Dialogue Group for the Evaluation of Cardiovascular Risk in Patients with Diabetes. Cardiac imaging for risk stratification in diabetes. Diabetes Care 2007;30:1295-304. https://doi.org/10.2337/dc06-2094
  3. Kamalesh M, Feigenbaum H, Sawada S. Assessing prognosis in patients with diabetes mellitus: the Achilles' heel of cardiac stress imaging tests? Am J Cardiol 2007;99:1016-9. https://doi.org/10.1016/j.amjcard.2006.10.071
  4. Elhendy A, Arruda AM, Mahoney DW, Pellikka PA. Prognostic stratification of diabetic patients by exercise echocardiography. J Am Coll Cardiol 2001;37:1551-7. https://doi.org/10.1016/S0735-1097(01)01199-8
  5. American College of Cardiology Foundation Task Force on Expert Consensus Documents, Mark DB, Berman DS, Budoff MJ, Carr JJ, Gerber TC, Hecht HS, Hlatky MA, Hodgson JM, Lauer MS, Miller JM, Morin RL, Mukherjee D, Poon M, Rubin GD, Schwartz RS. ACCF/ACR/AHA/NASCI/SAIP/SCAI/SCCT 2010 expert consensus document on coronary computed tomographic angiography: a report of the American College of Cardiology Foundation Task Force on Expert Consensus Documents. J Am Coll Cardiol 2010;55:2663-99. https://doi.org/10.1016/j.jacc.2009.11.013
  6. Park GM, Lee JH, Lee SW, Yun SC, Kim YH, Cho YR, Gil EH, Kim TS, Kim CJ, Cho JS, Park MW, Her SH, Yang DH, Kang JW, Lim TH, Koh EH, Lee WJ, Kim MS, Lee KU, Kim HK, Choe J, Park JY. Comparison of coronary computed tomographic angiographic findings in asymptomatic subjects with versus without diabetes mellitus. Am J Cardiol 2015;116:372-8. https://doi.org/10.1016/j.amjcard.2015.04.046
  7. Bild DE, Bluemke DA, Burke GL, Detrano R, Diez Roux AV, Folsom AR, Greenland P, Jacob DR Jr, Kronmal R, Liu K, Nelson JC, O'Leary D, Saad MF, Shea S, Szklo M, Tracy RP. Multi-Ethnic Study of Atherosclerosis: objectives and design. Am J Epidemiol 2002;156:871-81. https://doi.org/10.1093/aje/kwf113
  8. Perk J, De Backer G, Gohlke H, Graham I, Reiner Z, Verschuren M, Albus C, Benlian P, Boysen G, Cifkova R, Deaton C, Ebrahim S, Fisher M, Germano G, Hobbs R, Hoes A, Karadeniz S, Mezzani A, Prescott E, Ryden L, Scherer M, Syvanne M, Scholte op Reimer WJ, Vrints C, Wood D, Zamorano JL, Zannad F; European Association for Cardiovascular Prevention & Rehabilitation (EACPR); ESC Committee for Practice Guidelines (CPG). European guidelines on cardiovascular disease prevention in clinical practice (version 2012). The fifth joint task force of the European Society of Cardiology and other societies on cardiovascular disease prevention in clinical practice (constituted by representatives of nine societies and by invited experts). Eur Heart J 2012;33:1635-701. https://doi.org/10.1093/eurheartj/ehs092
  9. Wolk MJ, Bailey SR, Doherty JU, Douglas PS, Hendel RC, Kramer CM, Min JK, Patel MR, Rosenbaum L, Shaw LJ, Stainback RF, Allen JM; American College of Cardiology Foundation Appropriate Use Criteria Task Force. ACCF/AHA/ASE/ASNC/HFSA/HRS/SCAI/SCCT/SCMR/STS 2013 multimodality appropriate use criteria for the detection and risk assessment of stable ischemic heart disease: a report of the American College of Cardiology foundation appropriate use criteria task force, American Heart Association, American Society of Echocardiography, American Society of Nuclear Cardiology, Heart Failure Society of America, Heart Rhythm Society, Society for Cardiovascular Angiography and Interventions, Society of Cardiovascular Computed Tomography, Society for Cardiovascular Magnetic Resonance, and Society of Thoracic Surgeons. J Am Coll Cardiol 2014;63:380-406. https://doi.org/10.1016/j.jacc.2013.11.009
  10. Gobardhan SN, Dimitriu-Leen AC, van Rosendael AR, van Zwet EW, Roos CJ, Oemrawsingh PV, Kharagjitsingh AV, Jukema JW, Delgado V, Schalij MJ, Bax JJ, Scholte AJ. Prevalence by computed tomographic angiography of coronary plaques in South Asian and white patients with type 2 diabetes mellitus at low and high risk using four cardiovascular risk scores (UKPDS, FRS, ASCVD, and JBS3). Am J Cardiol 2017;119:705-11. https://doi.org/10.1016/j.amjcard.2016.11.029
  11. Bild DE, Detrano R, Peterson D, Guerci A, Liu K, Shahar E, Ouyang P, Jackson S, Saad MF. Ethnic differences in coronary calcification: the Multi-Ethnic Study of Atherosclerosis (MESA). Circulation 2005;111:1313-20. https://doi.org/10.1161/01.CIR.0000157730.94423.4B
  12. Wagenknecht LE, Divers J, Bertoni AG, Langefeld CD, Carr JJ, Bowden DW, Elbein SC, Shea S, Lewis CE, Freedman BI. Correlates of coronary artery calcified plaque in blacks and whites with type 2 diabetes. Ann Epidemiol 2011;21:34-41. https://doi.org/10.1016/j.annepidem.2010.10.007
  13. Park GM, Lee SW, Cho YR, Kim CJ, Cho JS, Park MW, Her SH, Ahn JM, Lee JY, Park DW, Kang SJ, Kim YH, Lee CW, Koh EH, Lee WJ, Kim MS, Lee KU, Kang JW, Lim TH, Park SW, Park SJ, Park JY. Coronary computed tomographic angiographic findings in asymptomatic patients with type 2 diabetes mellitus. Am J Cardiol 2014;113:765-71. https://doi.org/10.1016/j.amjcard.2013.11.028
  14. Scholte AJ, Schuijf JD, Kharagjitsingh AV, Jukema JW, Pundziute G, van der Wall EE, Bax JJ. Prevalence of coronary artery disease and plaque morphology assessed by multi-slice computed tomography coronary angiography and calcium scoring in asymptomatic patients with type 2 diabetes. Heart 2008;94: 290-5. https://doi.org/10.1136/hrt.2007.121921
  15. Park GM, Cho YR, Lee SW, Yun SC, Gil EH, Kim DW, Kim TS, Kim CJ, Cho JS, Park MW, Her SH, Kim YH, Yang DH, Kang JW, Lim TH, Jung CH, Koh EH, Lee WJ, Kim MS, Lee KU, Kim HK, Choe J, Park JY. Family history of diabetes and the risk of subclinical atherosclerosis. Diabetes Metab 2016;42:170-7. https://doi.org/10.1016/j.diabet.2015.09.004
  16. Mrgan M, Funck KL, Gaur S, Ovrehus KA, Dey D, Kusk MW, Norgaard BL, Gram JB, Olsen MH, Gram J, Sand NPR. High burden of coronary atherosclerosis in patients with a new diagnosis of type 2 diabetes. Diab Vasc Dis Res 2017;14:468-76. https://doi.org/10.1177/1479164117728014
  17. Wackers FJ. Asymptomatic patients with diabetes mellitus should be screened for coronary artery disease. J Nucl Cardiol 2006;13:609-15. https://doi.org/10.1016/j.nuclcard.2006.06.129
  18. Pundziute G, Schuijf JD, Jukema JW, Boersma E, de Roos A, van der Wall EE, Bax JJ. Prognostic value of multislice computed tomography coronary angiography in patients with known or suspected coronary artery disease. J Am Coll Cardiol 2007; 49:62-70. https://doi.org/10.1016/j.jacc.2006.07.070
  19. Min JK, Berman DS, Dunning A, Achenbach S, Al-Mallah M, Budoff MJ, Cademartiri F, Callister TQ, Chang HJ, Cheng V, Chinnaiyan K, Chow BJ, Cury R, Delago A, Feuchtner G, Hadamitzky M, Hausleiter J, Kaufmann P, Karlsberg RP, Kim YJ, Leipsic J, Lin FY, Maffei E, Plank F, Raff G, Villines T, Labounty TM, Shaw LJ. All-cause mortality benefit of coronary revascularization vs. medical therapy in patients without known coronary artery disease undergoing coronary computed tomographic angiography: results from CONFIRM (COronary CT Angiography EvaluatioN For Clinical Outcomes: An InteRnational Multicenter Registry). Eur Heart J 2012;33:3088-97. https://doi.org/10.1093/eurheartj/ehs315
  20. Nicholls SJ, Tuzcu EM, Kalidindi S, Wolski K, Moon KW, Sipahi I, Schoenhagen P, Nissen SE. Effect of diabetes on progression of coronary atherosclerosis and arterial remodeling: a pooled analysis of 5 intravascular ultrasound trials. J Am Coll Cardiol 2008;52:255-62. https://doi.org/10.1016/j.jacc.2008.03.051
  21. Anand DV, Lim E, Darko D, Bassett P, Hopkins D, Lipkin D, Corder R, Lahiri A. Determinants of progression of coronary artery calcification in type 2 diabetes role of glycemic control and inflammatory/vascular calcification markers. J Am Coll Cardiol 2007;50:2218-25. https://doi.org/10.1016/j.jacc.2007.08.032
  22. Kiramijyan S, Ahmadi N, Isma'eel H, Flores F, Shaw LJ, Raggi P, Budoff MJ. Impact of coronary artery calcium progression and statin therapy on clinical outcome in subjects with and without diabetes mellitus. Am J Cardiol 2013;111:356-61. https://doi.org/10.1016/j.amjcard.2012.09.033
  23. Ndrepepa G, Iijima R, Kufner S, Braun S, Cassese S, Byrne RA, Sorges J, Schulz-Schupke S, Hoppmann P, Fussaro M, Laugwitz KL, Schunkert H, Kastrati A. Association of progression or regression of coronary artery atherosclerosis with long-term prognosis. Am Heart J 2016;177:9-16. https://doi.org/10.1016/j.ahj.2016.03.016
  24. Saremi A, Moritz TE, Anderson RJ, Abraira C, Duckworth WC, Reaven PD; Veterans Affairs Diabetes Trial (VADT). Rates and determinants of coronary and abdominal aortic artery calcium progression in the Veterans Affairs Diabetes Trial (VADT). Diabetes Care 2010;33:2642-7. https://doi.org/10.2337/dc10-1388
  25. Kataoka Y, Yasuda S, Miyamoto Y, Sase K, Kosuge M, Kimura K, Yoshimasa Y, Miyazaki S; DIANA study investigators. Clinical predictors of atheroma progression despite optimal glycemic control in early-stage diabetic patients with coronary artery disease: insight from the DIANA study. J Atheroscler Thromb 2014;21:509-18. https://doi.org/10.5551/jat.21089
  26. De Bruyne B, Fearon WF, Pijls NH, Barbato E, Tonino P, Piroth Z, Jagic N, Mobius-Winckler S, Rioufol G, Witt N, Kala P, MacCarthy P, Engstrom T, Oldroyd K, Mavromatis K, Manoharan G, Verlee P, Frobert O, Curzen N, Johnson JB, Limacher A, Nuesch E, Juni P; FAME 2 Trial Investigators. Fractional flow reserve-guided PCI for stable coronary artery disease. N Engl J Med 2014;371:1208-17. https://doi.org/10.1056/NEJMoa1408758
  27. Tonino PA, Fearon WF, De Bruyne B, Oldroyd KG, Leesar MA, Ver Lee PN, Maccarthy PA, Van't Veer M, Pijls NH. Angiographic versus functional severity of coronary artery stenoses in the FAME study fractional flow reserve versus angiography in multivessel evaluation. J Am Coll Cardiol 2010;55:2816-21. https://doi.org/10.1016/j.jacc.2009.11.096
  28. Danad I, Raijmakers PG, Driessen RS, Leipsic J, Raju R, Naoum C, Knuuti J, Maki M, Underwood RS, Min JK, Elmore K, Stuijfzand WJ, van Royen N, Tulevski II, Somsen AG, Huisman MC, van Lingen AA, Heymans MW, van de Ven PM, van Kuijk C, Lammertsma AA, van Rossum AC, Knaapen P. Comparison of coronary CT angiography, SPECT, PET, and hybrid imaging for diagnosis of ischemic heart disease determined by fractional flow reserve. JAMA Cardiol 2017;2:1100-7. https://doi.org/10.1001/jamacardio.2017.2471
  29. Danad I, Szymonifka J, Twisk JWR, Norgaard BL, Zarins CK, Knaapen P, Min JK. Diagnostic performance of cardiac imaging methods to diagnose ischaemia-causing coronary artery disease when directly compared with fractional flow reserve as a reference standard: a meta-analysis. Eur Heart J 2017;38:991-8.
  30. Fox CS, Golden SH, Anderson C, Bray GA, Burke LE, de Boer IH, Deedwania P, Eckel RH, Ershow AG, Fradkin J, Inzucchi SE, Kosiborod M, Nelson RG, Patel MJ, Pignone M, Quinn L, Schauer PR, Selvin E, Vafiadis DK; American Heart Association Diabetes Committee of the Council on Lifestyle and Cardiometabolic Health; Council on Clinical Cardiology, Council on Cardiovascular and Stroke Nursing, Council on Cardiovascular Surgery and Anesthesia, Council on Quality of Care and Outcomes Research; American Diabetes Association. Update on prevention of cardiovascular disease in adults with type 2 diabetes mellitus in light of recent evidence: a scientific statement from the American Heart Association and the American Diabetes Association. Diabetes Care 2015;38:1777-803. https://doi.org/10.2337/dci15-0012
  31. Bansal S, Wackers FJ, Inzucchi SE, Chyun DA, Davey JA, Staib LH, Young LH; DIAD Study Investigators. Five-year outcomes in high-risk participants in the Detection of Ischemia in Asymptomatic Diabetics (DIAD) study: a post hoc analysis. Diabetes Care 2011;34:204-9. https://doi.org/10.2337/dc10-1194
  32. Muhlestein JB, Lappe DL, Lima JA, Rosen BD, May HT, Knight S, Bluemke DA, Towner SR, Le V, Bair TL, Vavere AL, Anderson JL. Effect of screening for coronary artery disease using CT angiography on mortality and cardiac events in high-risk patients with diabetes: the FACTOR-64 randomized clinical trial. JAMA 2014;312:2234-43. https://doi.org/10.1001/jama.2014.15825
  33. Turrini F, Scarlini S, Mannucci C, Messora R, Giovanardi P, Magnavacchi P, Cappelli C, Evandri V, Zanasi A, Romano S, Cavani R, Ghidoni I, Tondi S, Bondi M. Does coronary Atherosclerosis Deserve to be Diagnosed earlY in Diabetic patients? The DADDY-D trial. Screening diabetic patients for unknown coronary disease. Eur J Intern Med 2015;26:407-13. https://doi.org/10.1016/j.ejim.2015.05.006
  34. Min JK, Labounty TM, Gomez MJ, Achenbach S, Al-Mallah M, Budoff MJ, Cademartiri F, Callister TQ, Chang HJ, Cheng V, Chinnaiyan KM, Chow B, Cury R, Delago A, Dunning A, Feuchtner G, Hadamitzky M, Hausleiter J, Kaufmann P, Kim YJ, Leipsic J, Lin FY, Maffei E, Raff G, Shaw LJ, Villines TC, Berman DS. Incremental prognostic value of coronary computed tomographic angiography over coronary artery calcium score for risk prediction of major adverse cardiac events in asymptomatic diabetic individuals. Atherosclerosis 2014;232:298-304. https://doi.org/10.1016/j.atherosclerosis.2013.09.025
  35. Fujimoto S, Kondo T, Kodama T, Orihara T, Sugiyama J, Kondo M, Endo A, Fukazawa H, Nagaoka H, Oida A, Ikeda T, Yamazaki J, Takase S, Narula J. Coronary computed tomography angiography-based coronary risk stratification in subjects presenting with no or atypical symptoms. Circ J 2012;76:2419-25. https://doi.org/10.1253/circj.CJ-12-0157
  36. Park GM, An H, Lee SW, Cho YR, Gil EH, Her SH, Kim YH, Lee CW, Koh EH, Lee WJ, Kim MS, Lee KU, Kang JW, Lim TH, Park SW, Park SJ, Park JY. Risk score model for the assessment of coronary artery disease in asymptomatic patients with type 2 diabetes. Medicine (Baltimore) 2015;94:e508. https://doi.org/10.1097/MD.0000000000000508
  37. Min JK, Taylor CA, Achenbach S, Koo BK, Leipsic J, Norgaard BL, Pijls NJ, De Bruyne B. Noninvasive fractional flow reserve derived from coronary CT angiography: clinical data and scientific principles. JACC Cardiovasc Imaging 2015;8:1209-22. https://doi.org/10.1016/j.jcmg.2015.08.006
  38. Norgaard BL, Leipsic J, Gaur S, Seneviratne S, Ko BS, Ito H, Jensen JM, Mauri L, De Bruyne B, Bezerra H, Osawa K, Marwan M, Naber C, Erglis A, Park SJ, Christiansen EH, Kaltoft A, Lassen JF, Botker HE, Achenbach S; NXT Trial Study Group. Diagnostic performance of noninvasive fractional flow reserve derived from coronary computed tomography angiography in suspected coronary artery disease: the NXT trial (analysis of coronary blood flow using CT angiography: next steps). J Am Coll Cardiol 2014;63:1145-55. https://doi.org/10.1016/j.jacc.2013.11.043
  39. Leipsic J, Yang TH, Thompson A, Koo BK, Mancini GB, Taylor C, Budoff MJ, Park HB, Berman DS, Min JK. CT angiography (CTA) and diagnostic performance of noninvasive fractional flow reserve: results from the Determination of Fractional Flow Reserve by Anatomic CTA (DeFACTO) study. AJR Am J Roentgenol 2014;202:989-94. https://doi.org/10.2214/AJR.13.11441

Cited by

  1. Role of pregnancy hormones and hormonal interaction on the maternal cardiovascular system: a literature review vol.108, pp.8, 2019, https://doi.org/10.1007/s00392-019-01441-x
  2. Effects of Diabetes on Motor Recovery After Cerebral Infarct: A Diffusion Tensor Imaging Study vol.104, pp.9, 2018, https://doi.org/10.1210/jc.2018-02502
  3. Co‐expression of glycosylated aquaporin‐1 and transcription factor NFAT5 contributes to aortic stiffness in diabetic and atherosclerosis‐prone mice vol.24, pp.5, 2020, https://doi.org/10.1111/jcmm.14843
  4. Recent Updates on Vascular Complications in Patients with Type 2 Diabetes Mellitus vol.35, pp.2, 2018, https://doi.org/10.3803/enm.2020.35.2.260