Skip to main content

Advertisement

Log in

Application of Non-invasive Imaging in Inflammatory Disease Conditions to Evaluate Subclinical Coronary Artery Disease

  • Psoriatic Arthritis (J Scher, Section Editor)
  • Published:
Current Rheumatology Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

Traditional risk models, such as the Framingham risk score, fail to capture the increased cardiovascular disease risk seen in patients with chronic inflammatory diseases. This review will cover imaging modalities and their emerging applications in assessing subclinical cardiovascular disease for both research and clinical care in patients with chronic inflammatory diseases.

Recent Findings

Multiple imaging modalities have been studied to assess for subclinical cardiovascular disease via functional/physiologic, inflammatory, and anatomic assessment in patients with chronic inflammatory diseases.

Summary

The use of imaging to evaluate subclinical cardiovascular disease in patients with chronic inflammatory diseases has the potential to capture early sub-clinical atherosclerosis, to improve risk stratification of future cardiovascular events, and to guide effective disease management.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Willerson JT, Ridker PM. Inflammation as a Cardiovascular Risk Factor. Circulation. 2004;109:II–2.

    Google Scholar 

  2. Aviña-Zubieta JA, Choi HK, Sadatsafavi M, Etminan M, Esdaile JM, Lacaille D. Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. Arthritis Rheum. 2008;59:1690–7.

    PubMed  Google Scholar 

  3. Mehta NN, Yu Y, Pinnelas R, Krishnamoorthy P, Shin DB, Troxel AB, et al. Attributable risk estimate of severe psoriasis on major cardiovascular events. Am J Med. 2011;124:775.e1-6.

    PubMed  Google Scholar 

  4. Gelfand JM, Dommasch ED, Shin DB, Azfar RS, Kurd SK, Wang X, et al. The risk of stroke in patients with psoriasis. J Invest Dermatol. 2009;129:2411–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Gu M-M, Wang X-P, Cheng Q-Y, Zhao Y-L, Zhang T-P, Li B-Z, et al. A Meta-Analysis of Cardiovascular Events in Systemic Lupus Erythematosus. Immunol Invest. 2019:1–16.

  6. Bacon PA, Stevens RJ, Carruthers DM, Young SP, Kitas GD. Accelerated atherogenesis in autoimmune rheumatic diseases. Autoimmun Rev. 2002;1:338–47.

    CAS  PubMed  Google Scholar 

  7. Zeller CB, Appenzeller S. Cardiovascular Disease in Systemic Lupus Erythematosus: The Role of Traditional and Lupus Related Risk Factors. Curr Cardiol Rev. 2008;4:116–22.

    CAS  PubMed  PubMed Central  Google Scholar 

  8. Sinicato NA, da Silva Cardoso PA, Appenzeller S. Risk Factors in Cardiovascular Disease in Systemic Lupus Erythematosus. Curr Cardiol Rev. 2013;9:15–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  9. Gelfand JM, Neimann AL, Shin DB, Wang X, Margolis DJ, Troxel AB. Risk of myocardial infarction in patients with psoriasis. JAMA. 2006;296:1735–41.

    CAS  PubMed  Google Scholar 

  10. Mehta NN, Azfar RS, Shin DB, Neimann AL, Troxel AB, Gelfand JM. Patients with severe psoriasis are at increased risk of cardiovascular mortality: cohort study using the General Practice Research Database. Eur Heart J. 2010;31:1000–6.

    PubMed  Google Scholar 

  11. Goff DC, Lloyd-Jones DM, Bennett G, Coady S, D’Agostino RB, Gibbons R, 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:S49–73.

    PubMed  Google Scholar 

  12. Reriani MK, Lerman LO, Lerman A. Endothelial function as a functional expression of cardiovascular risk factors. Biomark Med. 2010;4:351–60.

    PubMed  PubMed Central  Google Scholar 

  13. Alam TA, Seifalian AM, Baker D. A review of methods currently used for assessment of in vivo endothelial function. Eur J Vasc Endovasc Surg Off J Eur Soc Vasc Surg. 2005;29:269–76.

    CAS  Google Scholar 

  14. Joannides R, Haefeli WE, Linder L, Richard V, Bakkali EH, Thuillez C, et al. Nitric oxide is responsible for flow-dependent dilatation of human peripheral conduit arteries in vivo. Circulation. 1995;91:1314–9.

    CAS  PubMed  Google Scholar 

  15. Celermajer DS. Reliable endothelial function testing: at our fingertips? Circulation. 2008;117:2428–30.

    PubMed  Google Scholar 

  16. Kuvin JT, Patel AR, Sliney KA, Pandian NG, Sheffy J, Schnall RP, et al. Assessment of peripheral vascular endothelial function with finger arterial pulse wave amplitude. Am Heart J. 2003;146:168–74.

    PubMed  Google Scholar 

  17. Bonetti PO, Pumper GM, Higano ST, Holmes DR, Kuvin JT, Lerman A. Noninvasive identification of patients with early coronary atherosclerosis by assessment of digital reactive hyperemia. J Am Coll Cardiol. 2004;44:2137–41.

    PubMed  Google Scholar 

  18. Targonski PV, Bonetti PO, Pumper GM, Higano ST, Holmes DR, Lerman A. Coronary endothelial dysfunction is associated with an increased risk of cerebrovascular events. Circulation. 2003;107:2805–9.

    PubMed  Google Scholar 

  19. Matsuzawa Y, Kwon T-G, Lennon RJ, Lerman LO, Lerman A. Prognostic Value of Flow-Mediated Vasodilation in Brachial Artery and Fingertip Artery for Cardiovascular Events: A Systematic Review and Meta-Analysis. J Am Heart Assoc. 2015;4.

  20. Charakida M, de Groot E, Loukogeorgakis SP, Khan T, Lüscher T, Kastelein JJ, et al. Variability and reproducibility of flow-mediated dilatation in a multicentre clinical trial. Eur Heart J. 2013;34:3501–7.

    PubMed  Google Scholar 

  21. Rubinshtein R, Kuvin JT, Soffler M, Lennon RJ, Lavi S, Nelson RE, et al. Assessment of endothelial function by non-invasive peripheral arterial tonometry predicts late cardiovascular adverse events. Eur Heart J. 2010;31:1142–8.

    PubMed  Google Scholar 

  22. Castellon X, Bogdanova V. Chronic Inflammatory Diseases and Endothelial Dysfunction. Aging Dis. 2016;7:81–9.

    PubMed  PubMed Central  Google Scholar 

  23. Chatterjee Adhikari M, Guin A, Chakraborty S, Sinhamahapatra P, Ghosh A. Subclinical atherosclerosis and endothelial dysfunction in patients with early rheumatoid arthritis as evidenced by measurement of carotid intima-media thickness and flow-mediated vasodilatation: an observational study. Semin Arthritis Rheum. 2012;41:669–75.

    CAS  PubMed  Google Scholar 

  24. Vaudo G, Marchesi S, Gerli R, Allegrucci R, Giordano A, Siepi D, et al. Endothelial dysfunction in young patients with rheumatoid arthritis and low disease activity. Ann Rheum Dis. 2004;63:31–5.

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Foster W, Lip GYH, Raza K, Carruthers D, Blann AD. An observational study of endothelial function in early arthritis. Eur J Clin Invest. 2012;42:510–6.

    CAS  PubMed  Google Scholar 

  26. Sandoo A. Veldhuijzen van Zanten JJCS, Metsios GS, Carroll D, Kitas GD. Vascular function and morphology in rheumatoid arthritis: a systematic review. Rheumatol Oxf Engl. 2011;50:2125–39.

    Google Scholar 

  27. Kiss E, Soltesz P, Der H, Kocsis Z, Tarr T, Bhattoa H, et al. Reduced flow-mediated vasodilation as a marker for cardiovascular complications in lupus patients. J Autoimmun. 2006;27:211–7.

    CAS  PubMed  Google Scholar 

  28. El-Magadmi M, Bodill H, Ahmad Y, Durrington PN, Mackness M, Walker M, et al. Systemic lupus erythematosus: an independent risk factor for endothelial dysfunction in women. Circulation. 2004;110:399–404.

    PubMed  Google Scholar 

  29. Piper MK, Raza K, Nuttall SL, Stevens R, Toescu V, Heaton S, et al. Impaired endothelial function in systemic lupus erythematosus. Lupus. 2007;16:84–8.

    CAS  PubMed  Google Scholar 

  30. Wright SA, O’Prey FM, Rea DJ, Plumb RD, Gamble AJ, Leahey WJ, et al. Microcirculatory hemodynamics and endothelial dysfunction in systemic lupus erythematosus. Arterioscler Thromb Vasc Biol. 2006;26:2281–7.

    CAS  PubMed  Google Scholar 

  31. Sari I, Okan T, Akar S, Cece H, Altay C, Secil M, et al. Impaired endothelial function in patients with ankylosing spondylitis. Rheumatol Oxf Engl. 2006;45:283–6.

    CAS  Google Scholar 

  32. Gonzalez-Juanatey C, Llorca J, Miranda-Filloy JA, Amigo-Diaz E, Testa A, Garcia-Porrua C, et al. Endothelial dysfunction in psoriatic arthritis patients without clinically evident cardiovascular disease or classic atherosclerosis risk factors. Arthritis Rheum. 2007;57:287–93.

    CAS  PubMed  Google Scholar 

  33. Bodnár N, Kerekes G, Seres I, Paragh G, Kappelmayer J, Némethné ZG, et al. Assessment of subclinical vascular disease associated with ankylosing spondylitis. J Rheumatol. 2011;38:723–9.

    PubMed  Google Scholar 

  34. Fang N, Jiang M, Fan Y. Association Between Psoriasis and Subclinical Atherosclerosis. Medicine (Baltimore) [Internet]. 2016 [cited 2019 Aug 13];95. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4902401/

  35. von Stebut E, Reich K, Thaçi D, Koenig W, Pinter A, Körber A, et al. Impact of Secukinumab on Endothelial Dysfunction and Other Cardiovascular Disease Parameters in Psoriasis Patients over 52 Weeks. J Invest Dermatol. 2019;139:1054–62.

    Google Scholar 

  36. Zieman SJ, Melenovsky V, Kass DA. Mechanisms, pathophysiology, and therapy of arterial stiffness. Arterioscler Thromb Vasc Biol. 2005;25:932–43.

    CAS  PubMed  Google Scholar 

  37. Cecelja M, Chowienczyk P. Role of arterial stiffness in cardiovascular disease. JRSM Cardiovasc Dis. 2012;1.

    Google Scholar 

  38. Laurent S, Cockcroft J, Van Bortel L, Boutouyrie P, Giannattasio C, Hayoz D, et al. Expert consensus document on arterial stiffness: methodological issues and clinical applications. Eur Heart J. 2006;27:2588–605.

    PubMed  Google Scholar 

  39. Kullo IJ, Malik AR. Arterial ultrasonography and tonometry as adjuncts to cardiovascular risk stratification. J Am Coll Cardiol. 2007;49:1413–26.

    PubMed  Google Scholar 

  40. Mitchell GF, Hwang S-J, Vasan RS, Larson MG, Pencina MJ, Hamburg NM, et al. Arterial stiffness and cardiovascular events: the Framingham Heart Study. Circulation. 2010;121:505–11.

    PubMed  PubMed Central  Google Scholar 

  41. Reference Values for Arterial Stiffness’ Collaboration. Determinants of pulse wave velocity in healthy people and in the presence of cardiovascular risk factors: “establishing normal and reference values.” Eur Heart J. 2010;31:2338–2350.

  42. Meaume S, Benetos A, Henry OF, Rudnichi A, Safar ME. Aortic pulse wave velocity predicts cardiovascular mortality in subjects >70 years of age. Arterioscler Thromb Vasc Biol. 2001;21:2046–50.

    CAS  PubMed  Google Scholar 

  43. Laurent S, Boutouyrie P, Asmar R, Gautier I, Laloux B, Guize L, et al. Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertens Dallas Tex 1979. 2001;37:1236–41.

    CAS  PubMed  Google Scholar 

  44. van Popele NM, Mattace-Raso FUS, Vliegenthart R, Grobbee DE, Asmar R, van der Kuip DAM, et al. Aortic stiffness is associated with atherosclerosis of the coronary arteries in older adults: the Rotterdam Study. J Hypertens. 2006;24:2371–6.

    PubMed  Google Scholar 

  45. Cruickshank K, Riste L, Anderson SG, Wright JS, Dunn G, Gosling RG. Aortic pulse-wave velocity and its relationship to mortality in diabetes and glucose intolerance: an integrated index of vascular function? Circulation. 2002;106:2085–90.

    PubMed  Google Scholar 

  46. Shoji T, Emoto M, Shinohara K, Kakiya R, Tsujimoto Y, Kishimoto H, et al. Diabetes mellitus, aortic stiffness, and cardiovascular mortality in end-stage renal disease. J Am Soc Nephrol JASN. 2001;12:2117–24.

    CAS  PubMed  Google Scholar 

  47. Kumar A, Hung OY, Piccinelli M, Eshtehardi P, Corban MT, Sternheim D, et al. Low Coronary Wall Shear Stress Is Associated With Severe Endothelial Dysfunction in Patients With Nonobstructive Coronary Artery Disease. JACC Cardiovasc Interv. 2018;11:2072–80.

    PubMed  PubMed Central  Google Scholar 

  48. Mäki-Petäjä KM, Hall FC, Booth AD, Wallace SML, Yasmin null, Bearcroft PWP, et al. Rheumatoid arthritis is associated with increased aortic pulse-wave velocity, which is reduced by anti-tumor necrosis factor-alpha therapy. Circulation. 2006;114:1185–92.

    PubMed  Google Scholar 

  49. Dzieża-Grudnik A, Sulicka J, Strach M, Siga O, Klimek E, Korkosz M, et al. Arterial stiffness is not increased in patients with short duration rheumatoid arthritis and ankylosing spondylitis. Blood Press. 2017;26:115–21.

    PubMed  Google Scholar 

  50. Taverner D, Paredes S, Ferré R, Masana L, Castro A, Vallvé J-C. Assessment of arterial stiffness variables in patients with rheumatoid arthritis: A mediation analysis. Sci Rep. 2019;9:1–8.

    CAS  Google Scholar 

  51. Ambrosino P, Tasso M, Lupoli R, Di Minno A, Baldassarre D, Tremoli E, et al. Non-invasive assessment of arterial stiffness in patients with rheumatoid arthritis: a systematic review and meta-analysis of literature studies. Ann Med. 2015;47:457–67.

    PubMed  Google Scholar 

  52. Bjarnegråd N, Bengtsson C, Brodszki J, Sturfelt G, Nived O, Länne T. Increased aortic pulse wave velocity in middle aged women with systemic lupus erythematosus. Lupus. 2006;15:644–50.

    PubMed  Google Scholar 

  53. Sabio JM, Vargas-Hitos JA, Martínez-Bordonado J, Navarrete-Navarrete N, Díaz-Chamorro A, Olvera-Porcel C, et al. Cumulated organ damage is associated with arterial stiffness in women with systemic lupus erythematosus irrespective of renal function. Clin Exp Rheumatol. 2016;34:53–7.

    PubMed  Google Scholar 

  54. Wang P, Mao Y-M, Zhao C-N, Liu L-N, Li X-M, Li X-P, et al. Increased Pulse Wave Velocity in Systemic Lupus Erythematosus: A Meta-Analysis. Angiology. 2018;69:228–35.

    PubMed  Google Scholar 

  55. Duivenvoorden R, de Groot E, Elsen BM, Laméris JS, van der Geest RJ, Stroes ES, et al. In vivo quantification of carotid artery wall dimensions: 3.0-Tesla MRI versus B-mode ultrasound imaging. Circ Cardiovasc Imaging. 2009;2:235–42.

    CAS  PubMed  Google Scholar 

  56. Den Ruijter HM, Peters SAE, Anderson TJ, Britton AR, Dekker JM, Eijkemans MJ, et al. Common carotid intima-media thickness measurements in cardiovascular risk prediction: a meta-analysis. JAMA. 2012;308:796–803.

    Google Scholar 

  57. Lorenz MW, Polak JF, Kavousi M, Mathiesen EB, Völzke H, Tuomainen T-P, et al. Carotid intima-media thickness progression to predict cardiovascular events in the general population (the PROG-IMT collaborative project): a meta-analysis of individual participant data. Lancet Lond Engl. 2012;379:2053–62.

    Google Scholar 

  58. Södergren A, Karp K, Boman K, Eriksson C, Lundström E, Smedby T, et al. Atherosclerosis in early rheumatoid arthritis: very early endothelial activation and rapid progression of intima media thickness. Arthritis Res Ther. 2010;12:R158.

    PubMed  PubMed Central  Google Scholar 

  59. Bissell L-A, Erhayiem B, Fent G, Hensor EMA, Burska A, Donica H, et al. Carotid artery volumetric measures associate with clinical ten-year cardiovascular (CV) risk scores and individual traditional CV risk factors in rheumatoid arthritis; a carotid-MRI feasibility study. Arthritis Res Ther. 2018;20:266.

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Henrot P, Foret J, Barnetche T, Lazaro E, Duffau P, Seneschal J, et al. Assessment of subclinical atherosclerosis in systemic lupus erythematosus: A systematic review and meta-analysis. Jt Bone Spine Rev Rhum. 2018;85:155–63.

    Google Scholar 

  61. Sharma SK, Rathi M, Sahoo S, Prakash M, Dhir V, Singh S. Assessment of premature atherosclerosis in systemic lupus erythematosus patients with and without nephritis. Lupus. 2016;25:525–31.

    CAS  PubMed  Google Scholar 

  62. Bańska-Kisiel K, Haberka M, Bergler-Czop B, Brzezińska-Wcisło L, Okopień B, Gąsior Z. Carotid intima-media thickness in patients with mild or moderate psoriasis. Adv Dermatol Allergol Dermatol Alergol. 2016;33:286–9.

    Google Scholar 

  63. Atzeni F, Sarzi-Puttini P, Sitia S, Tomasoni L, Gianturco L, Battellino M, et al. Coronary flow reserve and asymmetric dimethylarginine levels: new measurements for identifying subclinical atherosclerosis in patients with psoriatic arthritis. J Rheumatol. 2011;38:1661–4.

    CAS  PubMed  Google Scholar 

  64. Balci DD, Balci A, Karazincir S, Ucar E, Iyigun U, Yalcin F, et al. Increased carotid artery intima-media thickness and impaired endothelial function in psoriasis. J Eur Acad Dermatol Venereol JEADV. 2009;23:1–6.

    CAS  PubMed  Google Scholar 

  65. Contessa C, Ramonda R, Lo Nigro A, Modesti V, Lorenzin M, Puato M, et al. Subclinical atherosclerosis in patients with psoriatic arthritis: a case-control study. Preliminary data. Reumatismo. 2009;61:298–305.

    CAS  PubMed  Google Scholar 

  66. Kim SY, Yang HS, Lee YW, Choe YB, Ahn KJ. Evaluation of the Beta Stiffness Index and Carotid Intima-Media Thickness in Asian Patients With Psoriasis. Angiology. 2015;66:889–95.

    CAS  PubMed  Google Scholar 

  67. Gonzalez-Cantero A, Gonzalez-Cantero J, Sanchez-Moya AI, Perez-Hortet C, Arias-Santiago S, Schoendorff-Ortega C, et al. Subclinical atherosclerosis in psoriasis. Usefulness of femoral artery ultrasound for the diagnosis, and analysis of its relationship with insulin resistance. PloS One. 2019;14:e0211808.

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Tarkin JM, Joshi FR, Rudd JHF. PET imaging of inflammation in atherosclerosis. Nat Rev Cardiol. 2014;11:443–57.

    CAS  PubMed  Google Scholar 

  69. Rudd JHF, Narula J, Strauss HW, Virmani R, Machac J, Klimas M, et al. Imaging atherosclerotic plaque inflammation by fluorodeoxyglucose with positron emission tomography: ready for prime time? J Am Coll Cardiol. 2010;55:2527–35.

    PubMed  Google Scholar 

  70. Ogawa M, Nakamura S, Saito Y, Kosugi M, Magata Y. What can be seen by 18F-FDG PET in atherosclerosis imaging? The effect of foam cell formation on 18F-FDG uptake to macrophages in vitro. J Nucl Med Off Publ Soc Nucl Med. 2012;53:55–8.

    CAS  Google Scholar 

  71. Rudd JHF, Warburton EA, Fryer TD, Jones HA, Clark JC, Antoun N, et al. Imaging atherosclerotic plaque inflammation with [18F]-fluorodeoxyglucose positron emission tomography. Circulation. 2002;105:2708–11.

    CAS  PubMed  Google Scholar 

  72. Duivenvoorden R, Mani V, Woodward M, Kallend D, Suchankova G, Fuster V, et al. Relationship of serum inflammatory biomarkers with plaque inflammation assessed by FDG PET/CT: the dal-PLAQUE study. JACC Cardiovasc Imaging. 2013;6:1087–94.

    PubMed  Google Scholar 

  73. Figueroa AL, Abdelbaky A, Truong QA, Corsini E, MacNabb MH, Lavender ZR, et al. Measurement of arterial activity on routine FDG PET/CT images improves prediction of risk of future CV events. JACC Cardiovasc Imaging. 2013;6:1250–9.

    PubMed  Google Scholar 

  74. Tawakol A, Fayad ZA, Mogg R, Alon A, Klimas MT, Dansky H, et al. Intensification of statin therapy results in a rapid reduction in atherosclerotic inflammation: results of a multicenter fluorodeoxyglucose-positron emission tomography/computed tomography feasibility study. J Am Coll Cardiol. 2013;62:909–17.

    CAS  PubMed  Google Scholar 

  75. von Schulthess GK, Kuhn FP, Kaufmann P, Veit-Haibach P. Clinical positron emission tomography/magnetic resonance imaging applications. Semin Nucl Med. 2013;43:3–10.

    Google Scholar 

  76. Fernández-Friera L, Fuster V, López-Melgar B, Oliva B, Sánchez-González J, Macías A, et al. Vascular Inflammation in Subclinical Atherosclerosis Detected by Hybrid PET/MRI. J Am Coll Cardiol. 2019;73:1371–82.

    PubMed  Google Scholar 

  77. Mehta NN, Yu Y, Saboury B, Foroughi N, Krishnamoorthy P, Raper A, et al. Systemic and vascular inflammation in patients with moderate to severe psoriasis as measured by [18F]-fluorodeoxyglucose positron emission tomography-computed tomography (FDG-PET/CT): a pilot study. Arch Dermatol. 2011;147:1031–9.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. Mehta NN, Torigian DA, Gelfand JM, Saboury B, Alavi A. Quantification of atherosclerotic plaque activity and vascular inflammation using [18-F] fluorodeoxyglucose positron emission tomography/computed tomography (FDG-PET/CT). J Vis Exp JoVE. 2012:e3777.

  79. Rose S, Sheth NH, Baker JF, Ogdie A, Raper A, Saboury B, et al. A comparison of vascular inflammation in psoriasis, rheumatoid arthritis, and healthy subjects by FDG-PET/CT: a pilot study. Am J Cardiovasc Dis. 2013;3:273–8.

    PubMed  PubMed Central  Google Scholar 

  80. Naik HB, Natarajan B, Stansky E, Ahlman MA, Teague H, Salahuddin T, et al. Severity of Psoriasis Associates With Aortic Vascular Inflammation Detected by FDG PET/CT and Neutrophil Activation in a Prospective Observational Study. Arterioscler Thromb Vasc Biol [Internet]. 2015 [cited 2018 Sep 14]; Available from: https://www.ahajournals.org/doi/10.1161/ATVBAHA.115.306460

  81. Dey AK, Joshi AA, Chaturvedi A, Lerman JB, Aberra TM, Rodante JA, et al. Association Between Skin and Aortic Vascular Inflammation in Patients With Psoriasis: A Case-Cohort Study Using Positron Emission Tomography/Computed Tomography. JAMA Cardiol. 2017;2:1013–8.

    PubMed  Google Scholar 

  82. Groenendyk JW, Shukla P, Dey AK, Elnabawi YA, Aksentijevich M, Choi H, et al. Association of aortic vascular uptake of 18FDG by PET/CT and aortic wall thickness by MRI in psoriasis: a prospective observational study. Eur J Nucl Med Mol Imaging [Internet]. 2019;46:2488–95. https://doi.org/10.1007/s00259-019-04454-w.

    Article  Google Scholar 

  83. Gelfand JM, Shin DB, Alavi A, Torigian DA, Werner T, Papadopoulos M, et al. A Phase IV, Randomized, Double-Blind, Placebo-Controlled Crossover Study of the Effects of Ustekinumab on Vascular Inflammation in Psoriasis (the VIP-U trial). J Invest Dermatol [Internet]. 2019 [cited 2019 Aug 28]; Available from: http://www.sciencedirect.com/science/article/pii/S0022202X19325370

  84. Mehta NN, Shin DB, Joshi AA, Dey AK, Armstrong AW, Duffin KC, et al. Effect of Two Psoriasis Treatments on Vascular Inflammation and Novel Inflammatory Cardiovascular Biomarkers: A Randomized Placebo-Controlled Trial. Circ Cardiovasc Imaging. 2018;11:e007394.

    PubMed  PubMed Central  Google Scholar 

  85. Vascular Inflammation in Psoriasis - Apremilast - Full Text View - ClinicalTrials.gov [Internet]. [cited 2019 Aug 28]. Available from: https://clinicaltrials.gov/ct2/show/NCT03082729

  86. Study to Evaluate the Effect of Secukinumab Compared to Placebo on Aortic Vascular Inflammation in Subjects With Moderate to Severe Plaque Psoriasis - Study Results - ClinicalTrials.gov [Internet]. [cited 2019 Aug 28]. Available from: https://clinicaltrials.gov/ct2/show/results/NCT02690701

  87. Skeoch S, Cristinacce PLH, Williams H, Pemberton P, Xu D, Sun J, et al. Imaging atherosclerosis in rheumatoid arthritis: evidence for increased prevalence, altered phenotype and a link between systemic and localised plaque inflammation. Sci Rep. 2017;7:827.

    CAS  PubMed  PubMed Central  Google Scholar 

  88. Mäki-Petäjä KM, Elkhawad M, Cheriyan J, Joshi FR, Ostör AJK, Hall FC, et al. Anti-tumor necrosis factor-α therapy reduces aortic inflammation and stiffness in patients with rheumatoid arthritis. Circulation. 2012;126:2473–80.

    PubMed  Google Scholar 

  89. Geraldino-Pardilla L, Zartoshti A, Ozbek AB, Giles JT, Weinberg R, Kinkhabwala M, et al. Arterial Inflammation Detected With 18 F-Fluorodeoxyglucose-Positron Emission Tomography in Rheumatoid Arthritis. Arthritis Rheumatol Hoboken NJ. 2018;70:30–9.

    CAS  Google Scholar 

  90. Roivainen A, Hautaniemi S, Möttönen T, Nuutila P, Oikonen V, Parkkola R, et al. Correlation of 18F-FDG PET/CT assessments with disease activity and markers of inflammation in patients with early rheumatoid arthritis following the initiation of combination therapy with triple oral antirheumatic drugs. Eur J Nucl Med Mol Imaging. 2013;40:403–10.

    CAS  PubMed  Google Scholar 

  91. Haavisto M, Saraste A, Pirilä L, Hannukainen JC, Kalliokoski KK, Kirjavainen A, et al. Influence of triple disease modifying anti-rheumatic drug therapy on carotid artery inflammation in drug-naive patients with recent onset of rheumatoid arthritis. Rheumatol Oxf Engl. 2016;55:1777–85.

    CAS  Google Scholar 

  92. Carlucci PM, Purmalek MM, Dey AK, Temesgen-Oyelakin Y, Sakhardande S, Joshi AA, et al. Neutrophil subsets and their gene signature associate with vascular inflammation and coronary atherosclerosis in lupus. JCI Insight. 2018;3.

  93. Batty JA, Subba S, Luke P, Gigi LWC, Sinclair H, Kunadian V. Intracoronary Imaging in the Detection of Vulnerable Plaques. Curr Cardiol Rep. 2016;18:28.

    PubMed  PubMed Central  Google Scholar 

  94. Papadopoulou S-L, Neefjes LA, Schaap M, Li H-L, Capuano E, van der Giessen AG, et al. Detection and quantification of coronary atherosclerotic plaque by 64-slice multidetector CT: a systematic head-to- head comparison with intravascular ultrasound. Atherosclerosis. 2011;219:163–70.

    CAS  PubMed  Google Scholar 

  95. Fischer C, Hulten E, Belur P, Smith R, Voros S, Villines TC. Coronary CT angiography versus intravascular ultrasound for estimation of coronary stenosis and atherosclerotic plaque burden: a meta- analysis. J Cardiovasc Comput Tomogr. 2013;7:256–66.

    PubMed  Google Scholar 

  96. Greenland P, LaBree L, Azen SP, Doherty TM, Detrano RC. Coronary artery calcium score combined with Framingham score for risk prediction in asymptomatic individuals. JAMA. 2004;291:210–5.

    CAS  PubMed  Google Scholar 

  97. Detrano R, Guerci AD, Carr JJ, Bild DE, Burke G, Folsom AR, et al. Coronary calcium as a predictor of coronary events in four racial or ethnic groups. N Engl J Med. 2008;358:1336–45.

    CAS  PubMed  Google Scholar 

  98. Polonsky TS, McClelland RL, Jorgensen NW, Bild DE, Burke GL, Guerci AD, et al. Coronary Artery Calcium Score and Risk Classification for Coronary Heart Disease Prediction: The Multi-Ethnic Study of Atherosclerosis. JAMA J Am Med Assoc. 2010;303:1610–6.

    CAS  Google Scholar 

  99. Nasir K, Bittencourt MS, Blaha MJ, Blankstein R, Agatson AS, Rivera JJ, et al. Implications of Coronary Artery Calcium Testing Among Statin Candidates According to American College of Cardiology/American Heart Association Cholesterol Management Guidelines: MESA (Multi-Ethnic Study of Atherosclerosis). J Am Coll Cardiol. 2015;66:1657–68.

    CAS  PubMed  Google Scholar 

  100. Morteza N, Peter L, Erling F, Ward CS, Silvio L, John R, et al. From Vulnerable Plaque to Vulnerable Patient. Circulation. 2003;108:1664–72.

    Google Scholar 

  101. Motoyama S, Ito H, Sarai M, Kondo T, Kawai H, Nagahara Y, et al. Plaque Characterization by Coronary Computed Tomography Angiography and the Likelihood of Acute Coronary Events in Mid-Term Follow-Up. J Am Coll Cardiol. 2015;66:337–46.

    PubMed  Google Scholar 

  102. Plank F, Friedrich G, Dichtl W, Klauser A, Jaschke W, Franz W-M, et al. The diagnostic and prognostic value of coronary CT angiography in asymptomatic high-risk patients: a cohort study. Open Heart. 2014;1:e000096.

    PubMed  PubMed Central  Google Scholar 

  103. Williams MC, Moss AJ, Dweck M, Adamson PD, Alam S, Hunter A, et al. Coronary Artery Plaque Characteristics Associated With Adverse Outcomes in the SCOT-HEART Study. J Am Coll Cardiol. 2019;73:291–301.

    PubMed  PubMed Central  Google Scholar 

  104. Kolossváry M, Karády J, Kikuchi Y, Ivanov A, Schlett CL, Lu MT, et al. Radiomics versus Visual and Histogram-based Assessment to Identify Atheromatous Lesions at Coronary CT Angiography: An Ex Vivo Study. Radiology. 2019;190407.

  105. Sheahan M, Ma X, Paik D, Obuchowski NA, St Pierre S, Newman WP, et al. Atherosclerotic Plaque Tissue: Noninvasive Quantitative Assessment of Characteristics with Software-aided Measurements from Conventional CT Angiography. Radiology. 2018;286:622–31.

    PubMed  Google Scholar 

  106. Antonopoulos AS, Sanna F, Sabharwal N, Thomas S, Oikonomou EK, Herdman L, et al. Detecting human coronary inflammation by imaging perivascular fat. Sci Transl Med. 2017;9.

    PubMed  Google Scholar 

  107. Oikonomou EK, Marwan M, Desai MY, Mancio J, Alashi A, Centeno EH, et al. Non-invasive detection of coronary inflammation using computed tomography and prediction of residual cardiovascular risk (the CRISP CT study): a post-hoc analysis of prospective outcome data. The Lancet. 2018;392:929–39.

    Google Scholar 

  108. Kao AH, Wasko MCM, Krishnaswami S, Wagner J, Edmundowicz D, Shaw P, et al. C-reactive protein and coronary artery calcium in asymptomatic women with systemic lupus erythematosus or rheumatoid arthritis. Am J Cardiol. 2008;102:755–60.

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Giles JT, Szklo M, Post W, Petri M, Blumenthal RS, Lam G, et al. Coronary arterial calcification in rheumatoid arthritis: comparison with the Multi-Ethnic Study of Atherosclerosis. Arthritis Res Ther. 2009;11:R36.

    PubMed  PubMed Central  Google Scholar 

  110. Karpouzas GA, Malpeso J, Choi T-Y, Li D, Munoz S, Budoff MJ. Prevalence, extent and composition of coronary plaque in patients with rheumatoid arthritis without symptoms or prior diagnosis of coronary artery disease. Ann Rheum Dis. 2014;73:1797–804.

    PubMed  Google Scholar 

  111. Kiani AN, Vogel-Claussen J, Magder LS, Petri M. Noncalcified coronary plaque in systemic lupus erythematosus. J Rheumatol. 2010;37:579–84.

    PubMed  Google Scholar 

  112. Khan A, Arbab-Zadeh A, Kiani AN, Magder LS, Petri M. Progression of Noncalcified and Calcified Coronary Plaque by CT Angiography in SLE. Rheumatol Int. 2017;37:59–65.

    CAS  PubMed  Google Scholar 

  113. Lerman JB, Joshi AA, Chaturvedi A, Aberra TM, Dey AK, Rodante JA, et al. Coronary Plaque Characterization in Psoriasis Reveals High-Risk Features That Improve After Treatment in a Prospective Observational Study. Circulation. 2017;136:263–76.

    PubMed  PubMed Central  Google Scholar 

  114. Elnabawi YA, Dey AK, Goyal A, Groenendyk JW, Chung JH, Belur AD, et al. Coronary artery plaque characteristics and treatment with biologic therapy in severe psoriasis: results from a prospective observational study. Cardiovasc Res. 2019;115:721–8.

    CAS  PubMed  PubMed Central  Google Scholar 

  115. Elnabawi YA, Oikonomou EK, Dey AK, Mancio J, Rodante JA, Aksentijevich M, et al. Association of Biologic Therapy With Coronary Inflammation in Patients With Psoriasis as Assessed by Perivascular Fat Attenuation Index. JAMA Cardiol. 2019;

  116. Shen J, Wong K-T, Cheng IT, Shang Q, Li EK, Wong P, et al. Increased prevalence of coronary plaque in patients with psoriatic arthritis without prior diagnosis of coronary artery disease. Ann Rheum Dis. 2017;76:1237–44.

    CAS  PubMed  Google Scholar 

  117. Hecht HS, Narula J, Fearon WF. Fractional Flow Reserve and Coronary Computed Tomographic Angiography: A Review and Critical Analysis. Circ Res. 2016;119:300–16.

    CAS  PubMed  Google Scholar 

  118. Koo B-K, Erglis A, Doh J-H, Daniels DV, Jegere S, Kim H-S, et al. Diagnosis of ischemia-causing coronary stenoses by noninvasive fractional flow reserve computed from coronary computed tomographic angiograms. Results from the prospective multicenter DISCOVER-FLOW (Diagnosis of Ischemia-Causing Stenoses Obtained Via Noninvasive Fractional Flow Reserve) study. J Am Coll Cardiol. 2011;58:1989–97.

    PubMed  Google Scholar 

  119. Min JK, Leipsic J, Pencina MJ, Berman DS, Koo B-K, van Mieghem C, et al. Diagnostic accuracy of fractional flow reserve from anatomic CT angiography. JAMA. 2012;308:1237–45.

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Nørgaard BL, Leipsic J, Gaur S, Seneviratne S, Ko BS, Ito H, et al. 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.

    PubMed  Google Scholar 

  121. Kruk M, Wardziak Ł, Demkow M, Pleban W, Pręgowski J, Dzielińska Z, et al. Workstation-Based Calculation of CTA-Based FFR for Intermediate Stenosis. JACC Cardiovasc Imaging. 2016;9:690–9.

    PubMed  Google Scholar 

Download references

Acknowledgments

Nil.

Funding

Dr. Mehta is supported by a grant from the NIH, HL-06193-05

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Nehal N. Mehta.

Ethics declarations

Conflict of Interest

NNM is a full-time US government employee and has served as a consultant for Amgen,Eli Lilly, and Leo Pharma receiving grants/other payments; as a principal investigator and/or investigator for AbbVie, Celgene, Janssen Pharmaceuticals, Inc, and Novartis receiving grants and/or research funding and as a principal investigator for the National Institute of Health receiving grants and/or research funding. HC and DEU are funded by the NIH Medical Research Scholars Program, a public-private partnership supported jointly by the NIH and generous contributions to the Foundation for the NIH from the Doris Duke Charitable Foundation (DDCF Grant #2014194), Genentech, Elsevier, and other private donors. All other authors have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This article is part of the Topical Collection on Psoriatic Arthritis

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Choi, H., Uceda, D.E., Dey, A.K. et al. Application of Non-invasive Imaging in Inflammatory Disease Conditions to Evaluate Subclinical Coronary Artery Disease. Curr Rheumatol Rep 22, 1 (2020). https://doi.org/10.1007/s11926-019-0875-0

Download citation

  • Published:

  • DOI: https://doi.org/10.1007/s11926-019-0875-0

Keywords

Navigation