Journal of Nuclear Cardiology

, Volume 25, Issue 6, pp 1990–1998 | Cite as

Is coronary calcium scoring too late? Total body arterial calcium burden in patients without known CAD and normal MPI

  • Adel H. A. Allam
  • Randall C. Thompson
  • Michael A. EskanderEmail author
  • Mohamed A. Mandour Ali
  • Ayman Sadek
  • Chris J. Rowan
  • M. Linda Sutherland
  • James D. Sutherland
  • Bruno Frohlich
  • David E. Michalik
  • The HORUS research team
  • Caleb E. Finch
  • Jagat Narula
  • Gregory S. Thomas
  • L. Samuel Wann
Original Article



Patients with normal myocardial perfusion imaging (MPI) have a good prognosis. However, pre-clinical coronary and extracoronary atherosclerosis may exist in the absence of myocardial ischemia.


154 Egyptian patients (mean age 53 years) underwent whole-body non-contrast CT following normal MPI.


Atherosclerosis in the form of calcification was observed in ≥1 vascular bed in 115 of 154 (75%) patients. This included the iliofemoral (62%), abdominal aorta (53%), thoracic aorta (47%), coronary (47%), and carotid (25%) vascular beds. Mean total body calcium score was 3172 ± 530 AU. Extracoronary atherosclerosis in patients with a zero coronary artery calcium (CAC) score was common, occurring in the above-listed beds 42%, 36%, 29%, and 7% of the time, respectively. CAC was rarely present without iliofemoral or abdominal aortic calcification.


Quantitative assessment of calcification in different vascular beds demonstrates that extracoronary atherosclerosis is common in patients who have normal MPI. Atherosclerotic calcifications are most common in the iliofemoral arteries and abdominal aorta, which typically predate coronary calcifications. An imaging strategy to detect extracoronary atherosclerosis could lead to greater understanding of the natural history of atherosclerosis in its long pre-clinical phase and possibly to earlier preventive strategies.


Atherosclerosis Myocardial perfusion imaging X-ray computed tomography Coronary artery disease Abdominal aorta Calcium 





Abdominal aorta


Thoracic aorta


Carotid arteries


Total body calcium score


Coronary arteries



We thank statistician Kevin Kennedy, M.S. of the Saint Luke’s Mid America Heart Institute, Kansas City, MO, for his expert assistance.



Supplementary material

12350_2017_925_MOESM1_ESM.tif (1.5 mb)
Online Appendix Figure 1 Mean age of men and women without arterial calcification, one-to-two vascular beds with calcification, and calcification of greater than three vascular beds (TIFF 1579 kb)
12350_2017_925_MOESM2_ESM.tif (3.1 mb)
Online Appendix Figure 2 (A) Prevalence of calcification within three arterial beds based on the presence of calcium within the coronary and/or carotid artery vascular beds. (B) Mean calcium score within three arterial beds based on the presence of calcium within the coronary and/or carotid artery vascular beds. Values are mean ± SE. P < 0.001 between three groups (TIFF 3199 kb)
12350_2017_925_MOESM3_ESM.pptx (739 kb)
Supplementary material 3 (PPTX 739 kb)


  1. 1.
    Cohn JN. Prevention of cardiovascular disease. Trends Cardiovasc Med 2015;25:436-42.CrossRefGoogle Scholar
  2. 2.
    Wann S. Dying with cardiovascular disease, not of it. Trends Cardiovasc Med 2015;25:443-44.CrossRefGoogle Scholar
  3. 3.
    Naghavi M, Falk E, Hecht HS, et al. From vulnerable plaque to vulnerable patient–Part III: Executive summary of the screening for heart attack prevention and education (SHAPE) task force report. Am J Cardiol 2006;98:2H-15H.CrossRefGoogle Scholar
  4. 4.
    Thompson RC, Allam AH, Lombardi GP, et al. Atherosclerosis across 4000 years of human history: The Horus study of four ancient populations. The Lancet 2013;381:1211-22.CrossRefGoogle Scholar
  5. 5.
    Allam AH, Thompson RC, Wann L, Miyamoto MI, Thomas GS. Computed tomographic assessment of atherosclerosis in ancient egyptian mummies. JAMA 2009;302:2091-94.CrossRefGoogle Scholar
  6. 6.
    Allam AH, Thompson RC, Wann LS, et al. Atherosclerosis in ancient Egyptian mummies: The Horus study. JACC Cardiovasc Imaging 2011;4:315-27.CrossRefGoogle Scholar
  7. 7.
    Bild DE. Multi-ethnic study of atherosclerosis: Objectives and design. Am J Epidemiol 2002;156:871-81.CrossRefGoogle Scholar
  8. 8.
    Demer LL, Tintut Y. Vascular calcification: Pathobiology of a multifaceted disease. Circulation 2008;117:2938-48.CrossRefGoogle Scholar
  9. 9.
    Henzlova MJ, Duvall WL, Einstein AJ, Travin MI, Verberne HJ. ASNC imaging guidelines for SPECT nuclear cardiology procedures: Stress, protocols, and tracers. J Nucl Cardiol 2016;23:606-39.CrossRefGoogle Scholar
  10. 10.
    Hendel RC, Berman DS, Di Carli MF, et al. ACCF/ASNC/ACR/AHA/ASE/SCCT/SCMR/SNM 2009 Appropriate use criteria for cardiac radionuclide imaging: A Report of the American College of Cardiology Foundation Appropriate Use Criteria Task Force, the American Society of Nuclear Cardiology, the American College of Radiology, the American Heart Association, the American Society of Echocardiography, the Society of Cardiovascular Computed Tomography, the Society for Cardiovascular Magnetic Resonance, and the Society of Nuclear Medicine. J Am Coll Cardiol 2009;53:2201-29.CrossRefGoogle Scholar
  11. 11.
    Klocke FJ, Baird MG, Lorell BH, et al. ACC/AHA/ASNC guidelines for the clinical use of cardiac radionuclide imaging–executive summary: A report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (ACC/AHA/ASNC Committee to Revise the 1995 Guidelines for the Clinical Use of Cardiac Radionuclide Imaging). Circulation 2003;108:1404-18.CrossRefGoogle Scholar
  12. 12.
    Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte JM, Detrano R. Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 1990;15:827-32.CrossRefGoogle Scholar
  13. 13.
    Allison MA, Hsi S, Wassel CL, et al. Calcified atherosclerosis in different vascular beds and the risk of mortality. Arterioscler Thromb Vasc Biol 2012;32:140-46.CrossRefGoogle Scholar
  14. 14.
    Fernandez-Friera L, Penalvo JL, Fernandez-Ortiz A, et al. Prevalence, vascular distribution, and multiterritorial extent of subclinical atherosclerosis in a middle-aged cohort: The PESA (progression of early subclinical atherosclerosis) study. Circulation 2015;131:2104-13.CrossRefGoogle Scholar
  15. 15.
    Allison MA, Criqui MH, Wright CM. Patterns and risk factors for systemic calcified atherosclerosis. Arterioscler Thromb Vasc Biol 2004;24:331-36.CrossRefGoogle Scholar
  16. 16.
    Leherbauer L, Sonneck-Koenne C, Zakavi SR, et al. Coronary artery calcium (CAC) score—A prognostic tool in coronary artery disease? Iran J Nucl Med 2011;19:46-51.Google Scholar
  17. 17.
    Chang SM, Nabi F, Xu J, et al. The coronary artery calcium score and stress myocardial perfusion imaging provide independent and complementary prediction of cardiac risk. J Am Coll Cardiol 2009;54:1872-82.CrossRefGoogle Scholar
  18. 18.
    Chang SM, Nabi F, Xu J, et al. Value of CACS compared with ETT and myocardial perfusion imaging for predicting long-term cardiac outcome in asymptomatic and symptomatic patients at low risk for coronary disease: Clinical implications in a multimodality imaging world. JACC Cardiovasc Imaging 2015;8:134-44.CrossRefGoogle Scholar
  19. 19.
    Laclaustra M, Casasnovas JA, Fernández-Ortiz A, et al. Femoral and carotid subclinical atherosclerosis association with risk factors and coronary calcium: The AWHS study. J Am Coll Cardiol 2016;67:1263-74.CrossRefGoogle Scholar
  20. 20.
    Detrano R, Guerci AD, Carr JJ, et al. Coronary calcium as a predictor of coronary events in four racial or ethnic groups. N Engl J Med 2008;358:1336-45.CrossRefGoogle Scholar
  21. 21.
    Bos D, Ikram MA, Isaacs A, et al. Genetic loci for coronary calcification and serum lipids relate to aortic and carotid calcification. Circ Cardiovasc Genet 2013;6:47-53.CrossRefGoogle Scholar
  22. 22.
    Hacker M, Becker C. The incremental value of coronary artery calcium scores to myocardial single photon emission computer tomography in risk assessment. J Nucl Cardiol 2011;18:700-11 quiz 12-6.CrossRefGoogle Scholar
  23. 23.
    Schepis T, Gaemperli O, Koepfli P, et al. Added value of coronary artery calcium score as an adjunct to gated SPECT for the evaluation of coronary artery disease in an intermediate-risk population. J Nucl Med 2007;48:1424-30.CrossRefGoogle Scholar
  24. 24.
    Thompson RC, McGhie AI, Moser KW, et al. Clinical utility of coronary calcium scoring after nonischemic myocardial perfusion imaging. J Nucl Cardiol 2005;12:392-400.CrossRefGoogle Scholar
  25. 25.
    Wong ND, Gransar H, Shaw L, et al. Thoracic aortic calcium versus coronary artery calcium for the prediction of coronary heart disease and cardiovascular disease events. JACC Cardiovasc Imaging 2009;2:319-26.CrossRefGoogle Scholar
  26. 26.
    Arad Y, Spadaro LA, Roth M, Newstein D, Guerci AD. Treatment of asymptomatic adults with elevated coronary calcium scores with atorvastatin, vitamin C, and vitamin E: The St. Francis Heart Study randomized clinical trial. J Am Coll Cardiol 2005;46:166-72.CrossRefGoogle Scholar
  27. 27.
    Hwang IC, Jeon JY, Kim Y, et al. Statin therapy is associated with lower all-cause mortality in patients with non-obstructive coronary artery disease. Atherosclerosis 2015;239:335-42.CrossRefGoogle Scholar
  28. 28.
    Rozanski A, Gransar H, Shaw LJ, et al. Impact of coronary artery calcium scanning on coronary risk factors and downstream testing the EISNER (early identification of subclinical atherosclerosis by noninvasive imaging research) prospective randomized trial. J Am Coll Cardiol 2011;57:1622-32.CrossRefGoogle Scholar
  29. 29.
    Schenker MP, Dorbala S, Hong EC, et al. Interrelation of coronary calcification, myocardial ischemia, and outcomes in patients with intermediate likelihood of coronary artery disease: A combined positron emission tomography/computed tomography study. Circulation 2008;117:1693-700.CrossRefGoogle Scholar
  30. 30.
    Wayhs R, Zelinger A, Raggi P. High coronary artery calcium scores pose an extremely elevated risk for hard events. J Am Coll Cardiol 2002;39:225-30.CrossRefGoogle Scholar
  31. 31.
    Shah PK. Screening asymptomatic subjects for subclinical atherosclerosis: can we, does it matter, and should we? J Am Coll Cardiol 2010;56:98-105.CrossRefGoogle Scholar
  32. 32.
    Shah PK. Rapid detection of subclinical atherosclerosis: Potential implications for primary prevention in LMIC. Glob Heart 2013;8:91-3.CrossRefGoogle Scholar
  33. 33.
    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. J Am Coll Cardiol 2014;63:2889-934.CrossRefGoogle Scholar
  34. 34.
    Weintraub WS, Daniels SR, Burke LE, et al. Value of primordial and primary prevention for cardiovascular disease: A policy statement from the American Heart Association. Circulation 2011;124:967-90.CrossRefGoogle Scholar
  35. 35.
    Leppo JA. Comparison of pharmacologic stress agents. J Nucl Cardiol 1996;3:S22-26.CrossRefGoogle Scholar
  36. 36.
    Furtado CD, Aguirre DA, Sirlin CB, et al. Whole-body CT screening: Spectrum of findings and recommendations in 1192 patients. Radiology 2005;237:385-94.CrossRefGoogle Scholar

Copyright information

© American Society of Nuclear Cardiology 2017

Authors and Affiliations

  • Adel H. A. Allam
    • 1
    • 16
  • Randall C. Thompson
    • 2
    • 3
  • Michael A. Eskander
    • 4
    Email author
  • Mohamed A. Mandour Ali
    • 1
  • Ayman Sadek
    • 1
  • Chris J. Rowan
    • 5
  • M. Linda Sutherland
    • 6
  • James D. Sutherland
    • 7
  • Bruno Frohlich
    • 8
  • David E. Michalik
    • 9
    • 10
  • The HORUS research team
  • Caleb E. Finch
    • 11
  • Jagat Narula
    • 12
  • Gregory S. Thomas
    • 13
    • 14
  • L. Samuel Wann
    • 15
  1. 1.Al Azhar UniversityCairoEgypt
  2. 2.Saint Luke’s Mid America Heart InstituteKansas CityUSA
  3. 3.University of Missouri–Kansas City School of MedicineKansas CityUSA
  4. 4.University of California, Irvine HealthOrangeUSA
  5. 5.Renown Institute for Heart and Vascular HealthRenoUSA
  6. 6.Newport Diagnostic CenterNewportUSA
  7. 7.South Coast Radiological Medical GroupLaguna HillsUSA
  8. 8.National Museum of Natural History Smithsonian InstitutionWashington, DCUSA
  9. 9.University of CaliforniaIrvine School of MedicineIrvineUSA
  10. 10.Miller Women’s and Children’s HospitalLong BeachUSA
  11. 11.Leonard Davis School of Gerontology and Dornsife CollegeUniversity of Southern CaliforniaLos AngelesUSA
  12. 12.Icahn School of Medicine at Mount SinaiNew YorkUSA
  13. 13.Long Beach MemorialLong BeachUSA
  14. 14.University of California, IrvineOrangeUSA
  15. 15.Ascension HealthcareMilwaukeeUSA
  16. 16.Alpha ScanGizaEgypt

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