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Research ArticleArticle

Disease Activity in Ankylosing Spondylitis and Associations to Markers of Vascular Pathology and Traditional Cardiovascular Disease Risk Factors: A Cross-sectional Study

Inger Jorid Berg, Désirée van der Heijde, Hanne Dagfinrud, Ingebjørg Seljeflot, Inge Christoffer Olsen, Tore K. Kvien, Anne Grete Semb and Sella A. Provan
The Journal of Rheumatology April 2015, 42 (4) 645-653; DOI: https://doi.org/10.3899/jrheum.141018
Inger Jorid Berg
From the Department of Rheumatology, Diakonhjemmet Hospital, and Department of Cardiology, Center for Clinical Heart Research, Oslo University Hospital Ullevål, and University of Oslo, Oslo, Norway; Department of Rheumatology, Leiden University Medical Center, Leiden, the Netherlands.
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  • For correspondence: ingerjoridberg{at}gmail.com
Désirée van der Heijde
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Hanne Dagfinrud
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Ingebjørg Seljeflot
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Inge Christoffer Olsen
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Tore K. Kvien
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Anne Grete Semb
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Sella A. Provan
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  • Markers of vascular pathology in patients with ankylosing spondylitis (AS) who have high and low ASDAS, and controls. Linear regression models presented with estimated marginal means and 95% CI. aAdjusted for age, sex, BMI, current smoking, and creatinine. bAdjusted for age, sex, BMI, current smoking, CMAP, and height. cAdjusted for age, sex, BMI, current smoking, and CMAP. ASDAS: AS Disease Activity Score; ADMA: asymmetric dimethylarginine; BMI: body mass index; CMAP: central mean arterial pressure.
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    Figure 1.

    Markers of vascular pathology in patients with ankylosing spondylitis (AS) who have high and low ASDAS, and controls. Linear regression models presented with estimated marginal means and 95% CI. aAdjusted for age, sex, BMI, current smoking, and creatinine. bAdjusted for age, sex, BMI, current smoking, CMAP, and height. cAdjusted for age, sex, BMI, current smoking, and CMAP. ASDAS: AS Disease Activity Score; ADMA: asymmetric dimethylarginine; BMI: body mass index; CMAP: central mean arterial pressure.

  • Traditional cardiovascular risk factors in patients with ankylosing spondylitis (AS) who have high and low ASDAS, and controls. Linear regression models presented with estimated marginal means and 95% CI. aAdjusted for age, sex, BMI, current smoking, and use of statins. bAdjusted for age, sex, current smoking. cAdjusted for age, sex, BMI, current smoking, and use of antihypertensive. dAdjusted for age and sex, and presented with geometric mean; patients with CVD, diabetes, or outside the age range 40–65 years were excluded. eAdjusted for age and sex, and presented with geometric mean; patients with CVD or diabetes were excluded. ASDAS: AS Disease Activity Score; BMI: body mass index; BP: blood pressure; CVD: cardiovascular disease; HDL-C: high-density lipoprotein cholesterol; LDL-C: low-density lipoprotein cholesterol.
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    Figure 2.

    Traditional cardiovascular risk factors in patients with ankylosing spondylitis (AS) who have high and low ASDAS, and controls. Linear regression models presented with estimated marginal means and 95% CI. aAdjusted for age, sex, BMI, current smoking, and use of statins. bAdjusted for age, sex, current smoking. cAdjusted for age, sex, BMI, current smoking, and use of antihypertensive. dAdjusted for age and sex, and presented with geometric mean; patients with CVD, diabetes, or outside the age range 40–65 years were excluded. eAdjusted for age and sex, and presented with geometric mean; patients with CVD or diabetes were excluded. ASDAS: AS Disease Activity Score; BMI: body mass index; BP: blood pressure; CVD: cardiovascular disease; HDL-C: high-density lipoprotein cholesterol; LDL-C: low-density lipoprotein cholesterol.

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    Table 1.

    Characteristics of patients with ankylosing spondylitis (AS) and controls.

    CharacteristicsAS, n = 151Controls, n = 134
    AS, allAS, ASDAS ≥ 2.1, n = 73AS, ASDAS < 2.1, n = 69
    Demographic data
      Age, years, mean (SD)49.2 (11.1)a51.4 (10.4)d46.8 (11.2)c52.7 (11.4)
      Sex, male, n (%)92 (60.9)38 (52.1)d49 (71.0)78 (58.2)
      Smoking, current, n (%)30 (19.9)17 (23.3)10 (14.5)30 (22.6)
    Presence of comorbidities, n (%)
      Hypertension30 (19.9)14 (19.2)13 (18.8)30 (22.6)
      Diabetes8 (5.3)5 (6.8)2 (2.9)4 (3.0)
      CVD12 (7.9)9 (12.3)3 (4.3)7 (5.2)
    Current use of medication, n (%)
      Antihypertensive34 (22.5)18 (24.7)13 (18.8)28 (20.9)
      Statins18 (11.9)11 (15.1)7 (10.1)16 (11.9)
      NSAID99 (65.6)a47 (64.4)b46 (66.7)c17 (12.8)
      DMARD24 (16.0)12 (16.4)10 (14.5)NA
      TNF-α inhibitors29 (19.3)11 (15.1)18 (26.1)NA
      Prednisolone12 (7.9)a10 (13.7)b,d1 (1.4)3 (3.2)
    Disease characteristics
      Symptom duration, yrs, mean (SD)23.1 (10.5)25.4 (9.9)d20.3 (9.8)NA
      ASDAS, mean (SD)2.3 (1.0)3.0 (0.6)1.5 (0.5)NA
      BASDAI, mean (SD)3.7 (1.9)4.8 (1.6)d2.6 (1.3)NA
      HLA-B27–positive, n (%)120 (95.2)59 (96.7)55 (94.8)NA
      ESR, mm/h, median (IQR)17 (7–28)a23 (14–33)b,d11 (5–19)8 (4–14)
      CRP, mg/l, median (IQR)3 (1–10)a8 (4–18)b,d2 (1–3)1 (1–2)
    • Comparisons using bivariate tests as appropriate; Student t test for normally distributed data, Mann-Whitney U test for not normally distributed data, and chi-square test/Fisher’s test [when expected number was < 5 for at least 1 cell in ASDAS subgroups (diabetes and prednisolone)] for counts.

    • ↵a p value < 0.05, AS, all versus controls.

    • ↵b p value < 0.05, AS, ASDAS ≥ 2.1 versus controls.

    • ↵c p value < 0.05, AS, ASDAS < 2.1 versus controls.

    • ↵d p value < 0.05, AS, ASDAS ≥ 2.1 versus AS, ASDAS < 2.1. ASDAS: AS Disease Activity Score; BASDAI: Bath AS Disease Activity Index; CRP: C-reactive protein; CVD: cardiovascular disease; DMARD: disease-modifying antirheumatic drugs; ESR: erythrocyte sedimentation rate; NSAID: nonsteroidal antiinflammatory drugs; TNF-α: tumor necrosis factor-α; IQR: interquartile range.

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    Table 2.

    Markers of vascular pathology and traditional cardiovascular risk factors in patients with ankylosing spondylitis (AS) and controls.

    AS EMM (SE)Controls EMM (SE)Mean Difference (95% CI)p
    Markers of vascular pathology
      ADMA, µmol/la0.54 (0.01)0.49 (0.01)0.05 (0.03, 0.07)< 0.001
      Ratio L-arginine/ADMAa107 (2)117 (3)−10 (−16, −4)0.001
      AIx, %b19.4 (0.7)16.9 (0.7)2.6 (0.8, 4.3)0.01
      PWV, m/sc7.49 (0.12)7.55 (0.12)−0.06 (−0.35, 0.24)0.71
    Traditional CVD risk factors
      TC, mmol/ld5.07 (0.11)5.31 (0.12)−0.24 (−0.48, −0.01)0.04
      LDL-C, mmol/ld2.85 (0.10)3.11 (0.11)−0.26 (−0.47, −0.05)0.02
      HDL-C, mmol/ld1.53 (0.05)1.56 (0.05)−0.03 (−0.13, 0.07)0.54
      Ratio TC/HDL-Cd3.59 (0.14)3.65 (0.14)−0.06 (−0.35, 0.23)0.68
      BMI, kg/m2 e25.2 (0.3)25.5 (0.3)−0.3 (−1.2, 0.6)0.48
      Brachial SBP, mmHgf126 (2)127 (2)−1 (−5, 3)0.68
    CVD risk scores
      InEuropean Heart Score (+0.5)g0.63 (0.05)0.60 (0.05)0.03 (−0.11, 0.17)0.68
      InFramingham Risk Score (+0.5)h1.88 (0.04)1.89 (0.04)−0.01 (−0.13, 0.10)0.81
      InReynolds Risk Score (+0.5)h1.01 (0.05)0.96 (0.04)0.05 (−0.07, 0.18)0.42
    • Linear regression models presented with estimated marginal mean (EMM; SE) and estimated difference (95% CI).

    • ↵a Adjusted for age, sex, BMI, current smoking, creatinine.

    • ↵b Adjusted for age, sex, BMI, current smoking, CMAP, height.

    • ↵c Adjusted for age, sex, BMI, current smoking, CMAP.

    • ↵d Adjusted for age, sex, BMI, current smoking, use of statins.

    • ↵e Adjusted for age, sex, current smoking.

    • ↵f Adjusted for age, sex, BMI, current smoking, use of antihypertensive.

    • ↵g Adjusted for age, sex, and presented with geometric mean; patients with CVD, diabetes, or outside the age range 40–65 years were excluded.

    • ↵h Adjusted for age, sex, and presented with geometric mean; patients with CVD or diabetes were excluded. ADMA: asymmetric dimethylarginine; AIx: augmentation index; BMI: body mass index; CMAP: central mean arterial pressure; CVD: cardiovascular disease; HDL-C: high-density lipoprotein cholesterol; LDL-C: low-density lipoprotein cholesterol; PWV: pulse wave velocity; SBP: systolic blood pressure; TC: total cholesterol.

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Disease Activity in Ankylosing Spondylitis and Associations to Markers of Vascular Pathology and Traditional Cardiovascular Disease Risk Factors: A Cross-sectional Study
Inger Jorid Berg, Désirée van der Heijde, Hanne Dagfinrud, Ingebjørg Seljeflot, Inge Christoffer Olsen, Tore K. Kvien, Anne Grete Semb, Sella A. Provan
The Journal of Rheumatology Apr 2015, 42 (4) 645-653; DOI: 10.3899/jrheum.141018

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Disease Activity in Ankylosing Spondylitis and Associations to Markers of Vascular Pathology and Traditional Cardiovascular Disease Risk Factors: A Cross-sectional Study
Inger Jorid Berg, Désirée van der Heijde, Hanne Dagfinrud, Ingebjørg Seljeflot, Inge Christoffer Olsen, Tore K. Kvien, Anne Grete Semb, Sella A. Provan
The Journal of Rheumatology Apr 2015, 42 (4) 645-653; DOI: 10.3899/jrheum.141018
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Keywords

ANKYLOSING SPONDYLITIS
CARDIOVASCULAR DISEASE
DISEASE ACTIVITY
LIPOPROTEINS

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