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Original Article
Increased carotid atherosclerosis and carotid artery stiffness according to the disease duration and activity in patients with systemic lupus erythematosus
Gi Sup Byun1, Ji Hyun Lee1, Kyoung Im Cho2, HongJik Lee1, Hyun Jung Yeo1, Min Jeong Kim1, Ho Joon Im1
Kosin Medical Journal 2014;29(2):107-116.
DOI: https://doi.org/10.7180/kmj.2014.29.2.107
Published online: December 18, 2014

1Department of Internal Medicine, Maryknoll Medical Center, Busan, Korea

2Department of Internal Medicine, College of Medicine, Kosin University, Gospel Hospital, Busan, Korea

Corresponding Author : Kyoung Im Cho, Department of Internal Medicine, College of Medicine, Kosin University, 262, Kamcheon-ro, Seo-gu, Busan, 602-702, Korea TEL: +82-51-990-6990 FAX: +82-51-990-3049 E-mail: kyoungim74@gmail.com
• Received: April 9, 2013   • Accepted: September 11, 2013

Copyright © 2014 Kosin University School of Medicine Proceedings

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Objective:
    The ᅵink among carotid intimamedia thickness (IMT), vascular elastic property and the disease activity of systemic lupus erythematosus (SLE) is not well defined. We investigated the association between carotid atherosclerosis, elastic properties of the carotid arterial wall and clinical parameters of SLE.
  • Methods:
    Fifty-one SLE patients and fifty healthy controls were included. Peak systolic global circumferential and posterior radial strains of carotid artery were measured to assess the elastic properties. Beta stiffness index was used as conventional method for the distensibility of the carotid artery. Information concerning SLE duration, cumulative dose of steroids and/or immunosuppressive drug intake was recorded, and SLE activity was assessed by SLE disease activity index (SLEDAI) score.
  • Results:
    Carotid plaques were more common in SLE patients. SLE patients with plaques were 㢌der and showed the increased mean ᅵMT, high sensitivity C-reactive protein (hs CRP), IgG anti-cardi㢌ipin antibody (aCL), and longer disease duration compared with those without plaques. Peaksyst㢌ic global circumferential and posterior radial strain as well β stiffness index were significantly lower in SLE group. Age, disease duration, hsCRP, IgG aCL showed significant correlations with mean ᅵMT and parameters of carotid elastic property (all P's<0.05).
  • Conclusions:
    Carotid atherosclerosis was more common in SLE patients, and carotid arterial stiffness had significant correlation with disease duration, hsCRP and IgG aCL level. Speckle tracking strain imaging is a comparative method for the assessment of elastic properties of carotid artery of SLE patients.
  • Keywords: Carotid atherosclerosis; Strain; Systemic lupus erythematosus; Ultrasonography
Figure 1.
An automated tracking algorithm outlined the intima- media complex of common carotid artery (a). Systolic and diastolic diameters of common carotid artery were obtained from short axis view (b). Regions of interest with computation area of 1x1 mm were placed in the intimamedia complex from the short axis view of the common carotid artery (c and d). Peak systolic global circumferential strain (c) and posterior radial strain (d) and during systole were used for the analysis.
kmj-29-107f1.jpg
Table 1.
Clinical characteristics and parameters of the carotid artery of the study population
  SLE patients (n=51) Control (n=50) P
Age, yrs 47.5 ± 14.0 51.3± 10.1 0.122
Female, n (%) 32 (62.7 %) 29 {58 %) 0.841
BMI, kg/m 22.1±5.9 22.4 ± 4.9 0.683
Systolic blood pressure, mmHg 118.ftt 11.5 121.9 ± HU) 0.182
Diastolit Dlood pressure, mmHg 7L3 ± 10.4 73.8 ± 7.3 0.124
Total cholesterol, mg/dl 189.3 ±24.7 185.8 ±28.7 0.452
Mean IMT, mm 0.71 ±0.16 0.63 ± 0.09 0.04.1
Plaque, n (%) 14(27.5%) 3 (6%) <0.001
stiffness (β) 4.07 ± 0.73 3.69 ±0.53 0.004
Distmsibilily 0.37 ±0.10 0.45 ± 0.08 0.015
Conventional Strain, % 9.01±4.80 12.38 ± 5.52 0.002
Peak systolic global circumferential strain, % 3.61 ±1.25 6.23 ± 1.78 <0.001
Peak systolic posterior radial strain, % -3.96 ± 1.26 -4.75 ± 1.55 0.007

All values are presented as the mean ± SD

BMI body mass index, SLE systemic lupus erythematous, IMT intimamedia thickness

Table 2.
Characteristics of SLE patients with and without carotid arterial plaque
  SLE patients with plaques (0=14) SLE patients without plaques (n=37) P
Age, yrs 50.8 ± 14.1 45.6 ± 14.5 0.045
Disease duration, yis 9.23 ±4.34 4.64 ± 4.46 0.002
Total cholesterol, mg/dl 199.7 ±24.5 193.6 ±28.1 0.382
Systolic blood pressure, mmHg 113.8 ±7.6 11 ± 15.2 0.961
Diastolic blood pressure, mmHg 71.6 ± 6.4 71.2± 11.6 0.855
C-reactive proldn, mmol/L 4.01 ±5.62 0.47 ±0.57 <0.001
SLEDAI 4.93 ±4.42 6.35 ±6.53 0.421
Anti-dsDNA Ig G 27.9±51.9 23.6±50.5 0.794
Anti-dsDNA lgM 26.3±34.8 15.5±10,8 0.103
Anti Sm 20.2±56.2 20.5±65.8 0.984
Anti Ro 137.1±235.9 109.1 ± 188.9 0.665
Anti La 40.2±90.3 25.58±13.0 0.081
C3 98.7±58.6 70.2±52.5 0.126
C4 27.7 ± 16.1 18.9±12.2 0.064
Ig G aCI, 26.1 ±57.1 4.91 ± 10.8 0.0.16
Ig Μ aCI, 4.82±5.39 4.98±15.0 0.956
Mean IMT, mm 1.09±0.13 0.68 ±0,16 0.039
stiffness (β) 8..12 ± 7.32 3.iW±0.67 0.024
distensibility 0.3 2± 0.07 0.39±0.11 0.010
Conventional Strain, % 8.71 ±4,85 9.80 ±4.75 <0.001
Peak systolic global circumferential strain, % 2.90 ± 1.02 3.88 ± 1.22 0.008
Peak systolic posterior radial strain, % -3.42±0.94 -4.17 ± 132 0.0.11

All values are presented as the mean ± SD

SLE systemic lupus erythematous, SLEDAI Systemic Lupus Erythematosus Disease Activity Index, anti-dsDNA

Ab anti-double stranded DNA antibodies aCL anti-cardiolipin antibody, IMT intimamedia thickness

Table 3.
Correlation coefficients between the parameters of carotid artery and clinical parameters of SLE group (n=51)
  Mean IMT Beta stiffness index Distensibiljty
  r P r P r P
Agc 0.33 0.018 0.37 0.004 -0.22 0.037
Disease duration 0.43 0.002 0.24 0.023 -0.23 0.031
Systolic blood pressure 0.05 0.758 -0.19 0.171 -0.20 0.156
Diastolic blood pressure -0.03 0.863 0.07 0.951 >0.11 0.58
Total cholesterol 0.04 0.643 0.01 0.873 -0.10 0.37
hs CRP 0.49 <0.001 0.38 0.003 -0.26 0.008
IgG aCL 0.31 0.034 0.33 0.018 -0.17 0.102
SLEDAI 0.13 0.248 0.22 0.066 -0.11 0.297
  Peak systolic global circumferential strain Peak systolic posterior radial strain
  r P r P
Age -0.30 0.045 0.39 0.004
Disease duration -0.32 0.011 0.38 <0.001
Systolit blood pressure -0.31 0.030 0.37 0.008
Diaslolic blood pressure -0.17 0.232 0.23 0.111
Total cholesterol -0.12 0.325 0.19 0.254
hs CRP -0.23 0.035 0.27 0.027
IgG aCL -0.23 0.021 0.32 0.003
SLEDAI -0.19 0.372 0.17 0.298

IMT intimamedia thickness, hs CRP high sensitivity C-reactive protein, aCL anti-cardiolipin antibody, SLEDAI Systemic Lupus Erythematosus Disease Activity Index.

Table 4.
Multiple linear regression analysis of mean IMT and parameters of arterial stiffness of common carotid artery in SLE groups.
  Univariate analysis Multivariate analysis
Coefficient(β) P R2 Coefficient(β) P
Age 0.374 0.003 0.140 0.134 0.048
Disease duraiiun 0.257 0,072 0.066 0,110 0,035
Systolic blood pressure 0.046 0.753 0.002 0.041 ϋ.861
Diastolic blood pressure. -0.025 0.803 0 細 0.027 0.902
Total cholesterol 0.068 0.165 0.002 0.067 0.497
hsCRP 0.458 <0.001 0.209 0.486 0.004
SLEDAI 0.232 0.007 0.054 0.350 0.384
IgG aCL 0.094 0.516 0.009 -0.072 0.679
Mean IMT (R2 = 0.297, adjusted R2 = 0.143 in multivariute analysis)
Age 0.202 0.023 0.162 0,233 0.037
Disease duralion 0.433 0,002 0.188 0,454 0.033
Systolic blood pressure -0.005 0.421 0.000 0.075 0.716
Diastolic blood pressure, 0.021 0.033 0.000 0.052 0.800
Total cholesterol 0.104 0.471 0.011 0.038 0.693
hsCRP 0.480 >0.001 0.23 L 0.370 0.003
SLEDAJ 0.117 0.472 0.014 0.289 0.058
IgG aCL 0.298 0.086 0.089 0.167 0.513
Presence of plaque (R20.464, adjusted R2=0.347 in mullivariale analysis)
Age -0.285 0.045 0.081 -0.210 0.212
Disease ckiraiion -0.307 0.030 0.039 -0.410 0.008
Systolic blood pressure -0.172 0.232 0.030 -0.025 0.907
Diastolic blood pressure. -0.196 0.172 0.094 -0.393 0.067
Total cholcstcrol -0.120 0.238 0.014 -0.061 0.523
lisCRP -0.020 0.889 0.000 -0.192 0.262
SLEDAI -0.188 0.245 0.035 0.270 0.083
IgG aCL -0.046 0.75] 0.002 0.013 0.890
Peak systolic global circumferential strain(R2=0.442, adjusted R2=0.320 in multivariate Einalysis)
Age 0.433 <0.001 0.188 0.081 0.650
Disease duralion 0.156 0.281 0.024 0.208 0.045
Systolic bltxxi pressure. 0.197 0.185 0.039 0.274 0.231
Diastolic blood pressure, 0.009 0.952 0.000 -0.173 0.442
Total cholesterol 0.150 0.299 0.022 0.019 0.844
hsCRP 0.123 0.395 0.015 0.052 0.775
SLEDAI 0.224 0.036 0.179 0.269 0.057
IgG aCL 0.332 0.078 0.110 0.189 0.375
Beta stiffness index (R”=0..159, adjusted R2 =0.219 in inultivarialc analysis)

hs CRP high sensitivity C-reactive protein, SLEDAI Systemic Lupus Erythematosus Disease Activity Index, aCL anti-cardiolipin antibody.

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        Increased carotid atherosclerosis and carotid artery stiffness according to the disease duration and activity in patients with systemic lupus erythematosus
        Kosin Med J. 2014;29(2):107-116.   Published online December 18, 2014
        DOI: https://doi.org/10.7180/kmj.2014.29.2.107
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      Increased carotid atherosclerosis and carotid artery stiffness according to the disease duration and activity in patients with systemic lupus erythematosus
      Image
      Figure 1. An automated tracking algorithm outlined the intima- media complex of common carotid artery (a). Systolic and diastolic diameters of common carotid artery were obtained from short axis view (b). Regions of interest with computation area of 1x1 mm were placed in the intimamedia complex from the short axis view of the common carotid artery (c and d). Peak systolic global circumferential strain (c) and posterior radial strain (d) and during systole were used for the analysis.

      Figure 1.

      Increased carotid atherosclerosis and carotid artery stiffness according to the disease duration and activity in patients with systemic lupus erythematosus

      Clinical characteristics and parameters of the carotid artery of the study population

        SLE patients (n=51) Control (n=50) P
      Age, yrs 47.5 ± 14.0 51.3± 10.1 0.122
      Female, n (%) 32 (62.7 %) 29 {58 %) 0.841
      BMI, kg/m 22.1±5.9 22.4 ± 4.9 0.683
      Systolic blood pressure, mmHg 118.ftt 11.5 121.9 ± HU) 0.182
      Diastolit Dlood pressure, mmHg 7L3 ± 10.4 73.8 ± 7.3 0.124
      Total cholesterol, mg/dl 189.3 ±24.7 185.8 ±28.7 0.452
      Mean IMT, mm 0.71 ±0.16 0.63 ± 0.09 0.04.1
      Plaque, n (%) 14(27.5%) 3 (6%) <0.001
      stiffness (β) 4.07 ± 0.73 3.69 ±0.53 0.004
      Distmsibilily 0.37 ±0.10 0.45 ± 0.08 0.015
      Conventional Strain, % 9.01±4.80 12.38 ± 5.52 0.002
      Peak systolic global circumferential strain, % 3.61 ±1.25 6.23 ± 1.78 <0.001
      Peak systolic posterior radial strain, % -3.96 ± 1.26 -4.75 ± 1.55 0.007

      Characteristics of SLE patients with and without carotid arterial plaque

        SLE patients with plaques (0=14) SLE patients without plaques (n=37) P
      Age, yrs 50.8 ± 14.1 45.6 ± 14.5 0.045
      Disease duration, yis 9.23 ±4.34 4.64 ± 4.46 0.002
      Total cholesterol, mg/dl 199.7 ±24.5 193.6 ±28.1 0.382
      Systolic blood pressure, mmHg 113.8 ±7.6 11 ± 15.2 0.961
      Diastolic blood pressure, mmHg 71.6 ± 6.4 71.2± 11.6 0.855
      C-reactive proldn, mmol/L 4.01 ±5.62 0.47 ±0.57 <0.001
      SLEDAI 4.93 ±4.42 6.35 ±6.53 0.421
      Anti-dsDNA Ig G 27.9±51.9 23.6±50.5 0.794
      Anti-dsDNA lgM 26.3±34.8 15.5±10,8 0.103
      Anti Sm 20.2±56.2 20.5±65.8 0.984
      Anti Ro 137.1±235.9 109.1 ± 188.9 0.665
      Anti La 40.2±90.3 25.58±13.0 0.081
      C3 98.7±58.6 70.2±52.5 0.126
      C4 27.7 ± 16.1 18.9±12.2 0.064
      Ig G aCI, 26.1 ±57.1 4.91 ± 10.8 0.0.16
      Ig Μ aCI, 4.82±5.39 4.98±15.0 0.956
      Mean IMT, mm 1.09±0.13 0.68 ±0,16 0.039
      stiffness (β) 8..12 ± 7.32 3.iW±0.67 0.024
      distensibility 0.3 2± 0.07 0.39±0.11 0.010
      Conventional Strain, % 8.71 ±4,85 9.80 ±4.75 <0.001
      Peak systolic global circumferential strain, % 2.90 ± 1.02 3.88 ± 1.22 0.008
      Peak systolic posterior radial strain, % -3.42±0.94 -4.17 ± 132 0.0.11

      Correlation coefficients between the parameters of carotid artery and clinical parameters of SLE group (n=51)

        Mean IMT Beta stiffness index Distensibiljty
        r P r P r P
      Agc 0.33 0.018 0.37 0.004 -0.22 0.037
      Disease duration 0.43 0.002 0.24 0.023 -0.23 0.031
      Systolic blood pressure 0.05 0.758 -0.19 0.171 -0.20 0.156
      Diastolic blood pressure -0.03 0.863 0.07 0.951 >0.11 0.58
      Total cholesterol 0.04 0.643 0.01 0.873 -0.10 0.37
      hs CRP 0.49 <0.001 0.38 0.003 -0.26 0.008
      IgG aCL 0.31 0.034 0.33 0.018 -0.17 0.102
      SLEDAI 0.13 0.248 0.22 0.066 -0.11 0.297
        Peak systolic global circumferential strain Peak systolic posterior radial strain
        r P r P
      Age -0.30 0.045 0.39 0.004
      Disease duration -0.32 0.011 0.38 <0.001
      Systolit blood pressure -0.31 0.030 0.37 0.008
      Diaslolic blood pressure -0.17 0.232 0.23 0.111
      Total cholesterol -0.12 0.325 0.19 0.254
      hs CRP -0.23 0.035 0.27 0.027
      IgG aCL -0.23 0.021 0.32 0.003
      SLEDAI -0.19 0.372 0.17 0.298

      Multiple linear regression analysis of mean IMT and parameters of arterial stiffness of common carotid artery in SLE groups.

        Univariate analysis Multivariate analysis
      Coefficient(β) P R2 Coefficient(β) P
      Age 0.374 0.003 0.140 0.134 0.048
      Disease duraiiun 0.257 0,072 0.066 0,110 0,035
      Systolic blood pressure 0.046 0.753 0.002 0.041 ϋ.861
      Diastolic blood pressure. -0.025 0.803 0 細 0.027 0.902
      Total cholesterol 0.068 0.165 0.002 0.067 0.497
      hsCRP 0.458 <0.001 0.209 0.486 0.004
      SLEDAI 0.232 0.007 0.054 0.350 0.384
      IgG aCL 0.094 0.516 0.009 -0.072 0.679
      Mean IMT (R2 = 0.297, adjusted R2 = 0.143 in multivariute analysis)
      Age 0.202 0.023 0.162 0,233 0.037
      Disease duralion 0.433 0,002 0.188 0,454 0.033
      Systolic blood pressure -0.005 0.421 0.000 0.075 0.716
      Diastolic blood pressure, 0.021 0.033 0.000 0.052 0.800
      Total cholesterol 0.104 0.471 0.011 0.038 0.693
      hsCRP 0.480 >0.001 0.23 L 0.370 0.003
      SLEDAJ 0.117 0.472 0.014 0.289 0.058
      IgG aCL 0.298 0.086 0.089 0.167 0.513
      Presence of plaque (R20.464, adjusted R2=0.347 in mullivariale analysis)
      Age -0.285 0.045 0.081 -0.210 0.212
      Disease ckiraiion -0.307 0.030 0.039 -0.410 0.008
      Systolic blood pressure -0.172 0.232 0.030 -0.025 0.907
      Diastolic blood pressure. -0.196 0.172 0.094 -0.393 0.067
      Total cholcstcrol -0.120 0.238 0.014 -0.061 0.523
      lisCRP -0.020 0.889 0.000 -0.192 0.262
      SLEDAI -0.188 0.245 0.035 0.270 0.083
      IgG aCL -0.046 0.75] 0.002 0.013 0.890
      Peak systolic global circumferential strain(R2=0.442, adjusted R2=0.320 in multivariate Einalysis)
      Age 0.433 <0.001 0.188 0.081 0.650
      Disease duralion 0.156 0.281 0.024 0.208 0.045
      Systolic bltxxi pressure. 0.197 0.185 0.039 0.274 0.231
      Diastolic blood pressure, 0.009 0.952 0.000 -0.173 0.442
      Total cholesterol 0.150 0.299 0.022 0.019 0.844
      hsCRP 0.123 0.395 0.015 0.052 0.775
      SLEDAI 0.224 0.036 0.179 0.269 0.057
      IgG aCL 0.332 0.078 0.110 0.189 0.375
      Beta stiffness index (R”=0..159, adjusted R2 =0.219 in inultivarialc analysis)
      Table 1. Clinical characteristics and parameters of the carotid artery of the study population

      All values are presented as the mean ± SD

      BMI body mass index, SLE systemic lupus erythematous, IMT intimamedia thickness

      Table 2. Characteristics of SLE patients with and without carotid arterial plaque

      All values are presented as the mean ± SD

      SLE systemic lupus erythematous, SLEDAI Systemic Lupus Erythematosus Disease Activity Index, anti-dsDNA

      Ab anti-double stranded DNA antibodies aCL anti-cardiolipin antibody, IMT intimamedia thickness

      Table 3. Correlation coefficients between the parameters of carotid artery and clinical parameters of SLE group (n=51)

      IMT intimamedia thickness, hs CRP high sensitivity C-reactive protein, aCL anti-cardiolipin antibody, SLEDAI Systemic Lupus Erythematosus Disease Activity Index.

      Table 4. Multiple linear regression analysis of mean IMT and parameters of arterial stiffness of common carotid artery in SLE groups.

      hs CRP high sensitivity C-reactive protein, SLEDAI Systemic Lupus Erythematosus Disease Activity Index, aCL anti-cardiolipin antibody.

      Table 1.

      Table 2.

      Table 3.

      Table 4.

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