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Carotid Artery Stiffness Mechanisms in Hypertension and Their Association with Echolucency and Texture Features: The Multi-ethnic Study of Atherosclerosis (MESA)

  • Ryan Pewowaruk
    Correspondence
    Address correspondence to: Ryan Pewowaruk, William S. Middleton Memorial Veterans Hospital, 2400 Overlook Terrace, D2222, Madison, WI 53705, USA
    Affiliations
    Division of Cardiovascular Medicine, Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin, USA

    William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin, USA
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  • Claudia Korcarz
    Affiliations
    Division of Cardiovascular Medicine, Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin, USA
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  • Yacob Tedla
    Affiliations
    Division of Epidemiology, Department of Medicine, Vanderbilt University School of Medicine, Nashville, Tennessee, USA
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  • Carol Mitchell
    Affiliations
    Department of Medical Physics, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin, USA
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  • Adam D. Gepner
    Affiliations
    Division of Cardiovascular Medicine, Department of Medicine, University of Wisconsin School of Medicine and Public Health, Madison, Wisconsin, USA

    William S. Middleton Memorial Veterans Hospital, Madison, Wisconsin, USA
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      Abstract

      Arterial stiffness, echolucency and texture features are altered with hypertension and associated with increased cardiovascular disease risk. The relationship between these markers and structural and load-dependent artery wall changes in hypertension are poorly understood. The Multi-ethnic Study of Atherosclerosis (MESA) is a longitudinal study of 6814 adults from six communities across the United States designed to study subclinical cardiovascular disease. From B-mode imaging of the right common carotid artery at the baseline MESA examination, we calculated carotid artery Young's elastic modulus (YEM, n = 5894) and carotid artery gray-scale texture features (n = 1403). The standard YEM calculation represented total arterial stiffness. Structural stiffness was calculated by adjusting YEM to a standard blood pressure of 120/80 mm Hg with participant-specific models. Load-dependent stiffness was the difference between total and structural stiffness. We found that load-dependent YEM was elevated in hypertensive individuals compared with normotensive individuals (35.7 ± 105.5 vs. –62.0 ± 112.4 kPa, p < 0.001) but that structural YEM was similar (425.3 ± 274.8 vs. 428.4 ± 293.0 kPa, p = 0.60). Gray-scale measures of heterogeneity in carotid artery wall texture (gray-level difference statistic contrast) had small but statistically signification correlations with carotid artery stiffness mechanisms. This association was positive for structural YEM (0.107, p < 0.001), while for load-dependent YEM, the association was negative (–0.064, p = 0.02). In conclusion, increased arterial stiffness in hypertension was owing solely to the non-linear mechanics of having higher blood pressure, not structural changes in the artery wall, and high load-dependent stiffness was associated with a more homogenous carotid artery wall texture. This is potentially related to arterial remodeling associated with subclinical atherosclerosis and future cardiovascular disease development. These results also indicate that gray-scale texture features from ultrasound imaging had a small but statistically significant association with load-dependent arterial stiffness and that gray-scale texture features may be partially load dependent.

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      References

        • Andersson J
        • Sundström J
        • Gustavsson T
        • Hulthe J
        • Elmgren A
        • Zilmer K
        • Zilmer M
        • Lind L.
        Echogenecity of the carotid intima-media complex is related to cardiovascular risk factors, dyslipidemia, oxidative stress and inflammation. The Prospective Investigation of the Vasculature in Uppsala Seniors (PIVUS) study.
        Atherosclerosis. 2009; 204: 612-618
        • Bergel DH.
        The static elastic properties of the arterial wall.
        J Physiol. 1961; 156: 445-457
        • Bild DE
        • Bluemke DA
        • Burke GL
        • Detrano R
        • Diez Roux AV
        • Folsom AR
        • Greenland P
        • Jacobs DR
        • 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: 871-881
        • Blaha MJ
        • Budoff MJ
        • Rivera JJ
        • Katz R
        • O'Leary DH
        • Polak JF
        • Takasu J
        • Blumenthal RS
        • Nasir K
        Relationship of carotid distensibility and thoracic aorta calcification: Multi-ethnic study of atherosclerosis.
        Hypertension. 2009; 54: 1408-1415
        • Bramwell J
        • Hill A.
        The velocity of pulse wave in man.
        Proc R Soc Lond Ser B. 1922; 93: 298-306
        • Bussy C
        • Boutouyrie P
        • Lacolley P
        • Challande P
        • Laurent S.
        Intrinsic stiffness of the carotid arterial wall material in essential hypertensives.
        Hypertension. 2000; 35: 1049-1054
        • Doonan RJ
        • Gorgui J
        • Veinot JP
        • Lai C
        • Kyriacou E
        • Corriveau MM
        • Steinmetz OK
        • Daskalopoulou SS.
        Plaque echodensity and textural features are associated with histologic carotid plaque instability.
        J Vasc Surg. 2016; 64 (e8): 671-677
        • Duenwald S
        • Kobayashi H
        • Frisch K
        • Lakes R
        • Vanderby R.
        Ultrasound echo is related to stress and strain in tendon.
        J Biomech. 2011; 44: 424-429
        • Fung YC.
        Elasticity of soft tissues in simple elongation.
        Am J Physiol. 1967; 213: 1532-1544
        • Hayashi K
        • Handa H
        • Nagasawa S
        • Okumura A
        • Moritake K.
        Stiffness and elastic behavior of human intracranial and extracranial arteries.
        J Biomech. 1980; 13: 175-184
        • Hughes DS
        • Kelly JL.
        Second-order elastic deformation of solids.
        Phys Rev. 1953; 92: 1145-1149
        • Humphrey JD
        • Harrison DG
        • Figueroa CA
        • Lacolley P
        • Laurent S.
        Central artery stiffness in hypertension and aging a problem with cause and consequence.
        Circ Res. 2016; 118: 379-381
        • Jung M
        • Parrinello CM
        • Xue X
        • Mack WJ
        • Anastos K
        • Lazar JM
        • Selzer RH
        • Shircore AM
        • Plankey M
        • Tien P
        • Cohen M
        • Gange SJ
        • Hodis HN
        • Kaplan RC.
        Echolucency of the carotid artery intima-media complex and intima-media thickness have different cardiovascular risk factor relationships: The Women's Interagency HIV Study.
        J Am Heart Assoc. 2015; 4e001405
        • Korteweg DJ.
        Ueber die Fortpflanzungsgeschwindigkeit des Schalles in elastischen Röhren.
        Ann Phys. 1878; 241: 525-542
        • Lal BK
        • Hobson RW
        • Pappas PJ
        • Kubicka R
        • Hameed M
        • Chakhtura EY
        • Jamil Z
        • Padberg FT
        • Haser PB
        • Durán WN.
        Pixel distribution analysis of B-mode ultrasound scan images predicts histologic features of atherosclerotic carotid plaques.
        J Vasc Surg. 2002; 35: 1210-1217
        • Laurent S
        • Caviezel B
        • Beck L
        • Girerd X
        • Billaud E
        • Boutouyrie P
        • Hoeks A
        • Safar M.
        Carotid artery distensibility and distending pressure in hypertensive humans.
        Hypertension. 1994; 23: 878-883
        • Laurent S
        • Cockcroft J
        • Van Bortel L
        • Boutouyrie P
        • Giannattasio C
        • Hayoz D
        • Pannier B
        • Vlachopoulos C
        • Wilkinson I
        Struijker-Boudier H. Expert consensus document on arterial stiffness: Methodological issues and clinical applications.
        Eur Heart J. 2006; 27: 2588-2605
        • Lind L
        • Peters SAE
        • Den Ruijter HM
        • Palmer MK
        • Grobbee DE
        • Crouse JR
        • O'Leary DH
        • Evans GW
        • Raichlen JS
        • Bots ML
        Effect of rosuvastatin on the echolucency of the common carotid intima-media in low-risk individuals: The METEOR trial.
        J Am Soc Echocardiogr. 2012; 25 (e1): 1120-1127
        • Loizou CP
        • Pattichis CS
        • Pantziaris M
        • Kyriacou E
        • Nicolaides A.
        Texture feature variability in ultrasound video of the atherosclerotic carotid plaque.
        IEEE J Transl Eng Heal Med. 2017; 51800509
        • Mitchell CC
        • Stein JH
        • Cook TD
        • Salamat S
        • Wang X
        • Varghese T
        • Jackson DC
        • Sandoval Garcia C
        • Wilbrand SM
        • Dempsey RJ
        Histopathologic validation of grayscale carotid plaque characteristics related to plaque vulnerability.
        Ultrasound Med Biol. 2017; 43: 129-137
        • Mitchell CC
        • Korcarz CE
        • Tattersall MC
        • Gepner AD
        • Young RL
        • Post WS
        • Kaufman JD
        • McClelland RL
        • Stein JH.
        Carotid artery ultrasound texture, cardiovascular risk factors, and subclinical arterial disease: The multi-ethnic study of atherosclerosis (MeSA).
        Br J Radiol. 2018; 9120170637
        • Mitchell CC
        • Korcarz CE
        • Gepner AD
        • Nye R
        • Young RL
        • Matsuzaki M
        • Post WS
        • Kaufman JD
        • McClelland RL
        • Stein JH.
        Carotid artery echolucency, texture features, and incident cardiovascular disease events: The MESA study.
        J Am Heart Assoc. 2019; 8e010875
        • Moens AI.
        Die Pulscurve [The pulse curve].
        Leiden. 1878;
        • Nicolaides A
        • Sabetai M
        • Kakkos SK
        • Dhanjil S
        • Tegos T
        • Stevens JM
        • Thomas DJ
        • Francis S
        • Griffin M
        • Geroulakos G
        • Ioannidou E
        • Kyriacou E
        • Paaske W
        • Pagnan A
        • Pauletto P
        • Pagliara V
        • Pettina G
        • Pratesi C
        • Matticari S
        • Polivka J
        • Sevcik P
        • Poredos P
        • Blinc A
        • Videcnik V
        • Pujia A
        • Raso A
        • Rispoli P
        • Conforti M
        • Robinson T
        • Dennis MSJ
        • Rosfors S
        • Carlström C
        • Rudofsky G
        • Schroeder T
        • Gronholdt ML
        • Simoni G
        • Finocchi C
        • Rodriguez G
        • Spartera C
        • Ventura M
        • Scarpelli P
        • Sprynger M
        • Sadzot B
        • Hottermans C
        • Moonen G
        • Taylor PR
        • Tovar-Pardo A
        • Negreira J
        • Vayssairat M
        • Valaikiené J
        • Walker MG
        • Wilkinson AR.
        The Asymptomatic Carotid Stenosis and Risk of Stroke (ACSRS) study: Aims and result of quality control.
        Int Angiol. 2003; 22: 263-272
        • O'Rourke MF
        • Hashimoto J.
        Mechanical factors in arterial aging: A clinical perspective.
        J Am Coll Cardiol. 2007; 50: 1-13
        • Peters SAE
        • Lind L
        • Palmer MK
        • Grobbee DE
        • Crouse JR
        • O'Leary DH
        • Evans GW
        • Raichlen J
        • Bots ML
        • Den Ruijter HM
        Increased age, high body mass index and low HDL-C levels are related to an echolucent carotid intima-media: The METEOR study.
        J Intern Med. 2012; 272: 257-266
        • Pewowaruk RJ
        • Tedla Y
        • Korcarz CE
        • Tattersall MC
        • Stein JH
        • Chesler NC
        • Gepner AD.
        Carotid artery stiffening with aging: Structural versus load-dependent mechanisms in MESA (the Multi-ethnic Study of Atherosclerosis).
        Hypertension. 2022; 79: 150-158
        • Pewowaruk RJ
        • Korcarz C
        • Tedla Y
        • Burke G
        • Greenland P
        • Wu C
        • Gepner AD.
        Carotid artery stiffness mechanisms associated with cardiovascular disease events and incident hypertension: The MESA.
        Hypertension. 2022; 79: 659-666
        • Shirwany NA
        • Zou MH.
        Arterial stiffness: A brief review.
        Acta Pharmacol. 2010; 31: 1267-1276
        • Spronck B
        • Heusinkveld MHG
        • Vanmolkot FH
        • Roodt JO
        • Hermeling E
        • Delhaas T
        • Kroon AA
        • Reesink KD.
        Pressure-dependence of arterial stiffness.
        J Hypertens. 2015; 33: 330-338
        • Toupin RA
        • Bernstein B.
        Sound waves in deformed perfectly elastic materials: Acoustoelastic effect.
        J Acoust Soc Am. 1961; 33: 216-225
        • Townsend RR
        • Wilkinson IB
        • Schiffrin EL
        • Avolio AP
        • Chirinos JA
        • Cockcroft JR
        • Heffernan KS
        • Lakatta EG
        • McEniery CM
        • Mitchell GF
        • Najjar SS
        • Nichols WW
        • Urbina EM
        • Weber T.
        Recommendations for improving and standardizing vascular research on arterial stiffness: A Scientific Statement from the American Heart Association.
        Hypertension. 2015; 66: 698-722
        • Van Der Bruggen M
        • Spronck B
        • Bos S
        • Heusinkveld MHG
        • Taddei S
        • Ghiadoni L
        • Delhaas T
        • Bruno RM
        • Reesink KD.
        Pressure-corrected carotid stiffness and Young's modulus: Evaluation in an outpatient clinic setting.
        Am J Hypertens. 2021; 34: 737-743
        • Vlachopoulos C
        • Aznaouridis K
        • Stefanadis C.
        Prediction of cardiovascular events and all-cause mortality with arterial stiffness: A systematic review and meta-analysis.
        J Am Coll Cardiol. 2010; 55: 1318-1327
        • Whelton PK
        • Carey RM
        • Aronow WS
        • Casey DE
        • Collins KJ
        • Dennison Himmelfarb C
        • DePalma SM
        • Gidding S
        • Jamerson KA
        • Jones DW
        • MacLaughlin EJ
        • Muntner P
        • Ovbiagele B
        • Smith SC
        • Spencer CC
        • Stafford RS
        • Taler SJ
        • Thomas RJ
        • Williams KA
        • Williamson JD
        • Wright JT
        2017 ACC/AHA/AAPA/ABC/ACPM/AGS/APhA/ASH/ASPC/NMA/PCNA Guideline for the Prevention, Detection, Evaluation, and Management of High Blood Pressure in Adults: A Report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice.
        J Am Coll Cardiol. 2018; 71: e127-e248
        • Wohlin M
        • Sundström J
        • Andrén B
        • Larsson A
        • Lind L.
        An echolucent carotid artery intima–media complex is a new and independent predictor of mortality in an elderly male cohort.
        Atherosclerosis. 2009; 205: 486-491