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

Article information

Kosin Med J. 2014;29(2):107-116

Publication date (electronic) : 2014 December 18

doi : https://doi.org/10.7180/kmj.2014.29.2.107

Gi Sup Byun ¹, Ji Hyun Lee ¹, Kyoung Im Cho ²^,, HongJik Lee ¹, Hyun Jung Yeo ¹, Min Jeong Kim ¹, Ho Joon Im ¹

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 2013 April 09; 2013 July 19; Accepted 2013 September 11.

Abstract

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.

Table 1.

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

Table 2.

Characteristics of SLE patients with and without carotid arterial plaque

Table 3.

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

Table 4.

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

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Figure 1.

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.