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Clinical and serological associations of autoantibodies in patients with systemic lupus erythematosus

María Correa-Rodríguez, Gabriela Pocovi-Gerardino, Jose Luis Callejas-Rubio, Raquel Ríos-Fernández, María Martín-Amada, María-Gracia Cruz-Caparrós, Blanca Rueda-Medina, Norberto Ortego-Centeno
DOI: 10.1136/jim-2021-001887 Published 25 November 2021
María Correa-Rodríguez
1 Department of Nursing, Faculty of Health Sciences, University of Granada, Granada, Spain
2 Institute for Biosanitary Research of Granada (ibs.GRANADA), Granada, Spain
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Gabriela Pocovi-Gerardino
2 Institute for Biosanitary Research of Granada (ibs.GRANADA), Granada, Spain
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Jose Luis Callejas-Rubio
2 Institute for Biosanitary Research of Granada (ibs.GRANADA), Granada, Spain
3 Systemic Autoimmune Diseases Unit, San Cecilio University Hospital, Granada, Spain
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Raquel Ríos-Fernández
2 Institute for Biosanitary Research of Granada (ibs.GRANADA), Granada, Spain
3 Systemic Autoimmune Diseases Unit, San Cecilio University Hospital, Granada, Spain
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María Martín-Amada
4 Systemic Autoimmune Diseases Unit, Hospital of Jaén, Jaén, Spain
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María-Gracia Cruz-Caparrós
5 Systemic Autoimmune Diseases Unit, Hospital de Poniente, Almería (El Ejido), Spain
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Blanca Rueda-Medina
1 Department of Nursing, Faculty of Health Sciences, University of Granada, Granada, Spain
2 Institute for Biosanitary Research of Granada (ibs.GRANADA), Granada, Spain
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Norberto Ortego-Centeno
2 Institute for Biosanitary Research of Granada (ibs.GRANADA), Granada, Spain
6 Department of Medicine, University of Granada, Granada, Spain
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Article Figures & Data

Tables

  • Table 1

    Descriptive characteristics and clinical manifestations of the study population

    CharacteristicsTotal (n=264)
    Female265 (90.4)
    Age (years)46.87 (12.94)
    Time since diagnosis (years)9.12 (6.58)
    Smoking67 (22.9)
    Clinical activity
     SLEDAI score2.77±2.83
     SDI score1.00±1.25
    Laboratory data
     WBC (/µL)5709.86±2242.28
     Lymphocyte (/µL)1629.91±757.93
     Hemoglobin (/µL)13.89±6.61
     Platelet (x1000 /µL)226.44±70.64
     ESR (mm/h)19.24±15.50
     hs-CRP (mg/dL)3.23±4.89
     Hcy (µmol/L)12.44±7.25
     Albumin (g/dL)4.08±0.37
     AST (IU/L)23.71±10.80
     ALT (IU/L)19.69±9.47
     Complement C3 level (mg/dL)109.23±28.01
     Complement C4 level (mg/dL)22.80±16.69
    Medication used
     Antimalarial use231 (79.4)
     Immunosuppressor use107 (36.8)
     Corticoid use114 (39.2)
    Clinical manifestations
     Arthritis155 (55.6)
     Facial rash150 (53.8)
     Discoid lupus37 (13.3)
     Mucosal ulceration145 (52.0)
     Photosensitivity189 (67.7)
     Hemolytic anemia19 (6.8)
     Leukopenia168 (60.2)
     Thrombocytopenia41 (14.7)
     Neurological37 (13.3)
     Nephritis73 (26.2)
     Serositis36 (12.9)
    • Data are expressed as mean and frequency and percentage.

    • ALT, alanine transaminase; AST, aspartate transaminase; ESR, erythrocyte sedimentation rate; Hcy, homocysteine; hs-CRP, high-sensitivity C reactive protein; SDI, Systemic Lupus International Collaborating Clinics/American College of Rheumatology Damage Index; SLEDAI, Systemic Lupus Erythematosus Disease Activity Index; WBC, white blood cell.

  • Table 2

    Antinuclear antibodies in patients with SLE stratified according to sex and onset of the disease

    TotalTotal
    N (%)
    SexOnset of the disease
    Women, n (%)Men, n (%)P valueEarly onset <50 years, n (%)Late onset 50 years, n (%)P value
    Nucleosome31 (11.2)30 (12.0)1 (3.7)0.40618 (10.5)13 (12.1)0.406
    dsDNA (+)204 (71.3)183 (70.9)21 (75.0)0.651135 (77.1)69 (62.2) 0.006
    Sm (+)35 (12.0)32 (12.2)3 (10.7)0.82222 (12.4)13 (11.5)0.827
    RNP (+)30 (10.6)28 (10.6)2 (7.1)0.80122 (12.3)8 (7.1)0.257
    Ro (+)108 (37)103 (39.0)5 (17.9) 0.027 61 (34.1)47 (41.6)0.195
    La (+)27 (9.2)27 (10.2)–0.07613 (7.3)14 (12.4)0.141
    • Data are expressed as frequency and percentage.

    • Bold values denote statistical significance (p<0.05).

    • dsDNA, double-stranded DNA; RNP, ribonucleoprotein; SLE, systemic lupus erythematosus; Sm, Smith.

  • Table 3

    Clinical SLE disease activity and laboratory data in relation to autoantibody phenotype

    Nucleosome (+)
    (n=31)
    Nucleosome (−)
    (n=247)
    P valuedsDNA (+)
    (n=204)
    dsDNA (−)
    (n=82)
    P valueSm (+)
    (n=35)
    Sm (−)
    (n=256)
    P valueRNP (+)
    (n=31)
    RNP (−)
    (n=261)
    P valueRo (+)
    (n=108)
    Ro (−)
    (n=184)
    P valueLa (+) (n=27)La (−)
    (n=265)
    P value
    Clinical activity
    SLEDAI score3.87±2.722.52±2.76 0.004 3.08±2.912.04±2.48 0.010 3.14±2.762.73±2.840.4493.63±3.052.69±2.800.1492.60±2.732.87±2.890.4532.89±2.572.76±2.860.852
    SDI score1.61±1.990.89±1.06 0.004 1.03±1.320.93±1.090.1621.28±1.540.97±1.210.1231.26±1.550.98±1.220.2780.84±1.161.10±1.30 0.028 1.07±1.351.00±1.250.927
    Laboratory data
    WBC (/µL)5577.22±1723.925689.36±2210.660.8065814.12±2204.765507.53±2350.520.3155663.05±2141.015708.07±2260.520.9245383.79±1526.575738.30±2308.640.4555372.88±2001.315907.97±2355.390.0955321.92±2076.005748.21±2258.120.441
    Lymphocyte (/µL)1702.35±708.691628.45±764.860.7771624.28±793.941634.46±667.690.8681471.58±701.361651.70±764.150.1971314.93±569.461666.15±769.33 0.023 1530.43±671.791689.25±800.910.0871495.11±521.381644.24±778.260.335
    Hemoglobin (/µL)13.08±1.4514.02±7.170.79713.89±7.8313.89±1.040.98913.62±1.4113.93±7.040.79413.06±1.2513.99±6.970.78813.40±1.2214.18±8.280.36213.12±1.1613.97±6.920.589
    Platelet (×1000 /µL)228.19±54.85226.00±72.810.998226.43±71.48226.59±70.120.644211.97±58.12227.76±71.410.195224.20±58.87226.05±71.320.090232.79±68.57222.69±71.750.146258.55±68.78223.16±70.13 0.014
    ESR (mm/hour)25.60±18.8618.33±14.61 0.039 20.74±16.9415.53±10.71 0.015 21.37±18.7518.85±14.960.34027.06±18.4018.22±14.84 0.008 21.57±16.2617.84±14.90 0.042 23.34±17.3318.83±15.280.177
    hs-CRP (mg/dL)4.11±3.723.20±5.080.0783.61±5.502.37±2.82 0.030 3.21±4.923.25±4.900.9384.12±5.593.14±4.810.5563.44±6.143.11±3.990.4155.34±10.403.03±3.93 0.017
    Hcy (µmol/L)11.65±3.3612.65±7.760.58411.74±4.6914.18±11.18 0.023 11.80±4.0912.54±7.580.64212.57±4.3412.44±7.520.88612.41±5.6212.46±8.080.95513.69±9.4912.32±7.910.348
    Albumin (g/dL)3.98±0.404.09±0.370.4984.04±0.354.14±0.40 0.027 4.04±0.374.08±0.370.5963.98±0.344.09±0.380.2294.14±0.364.04±0.38 0.034 4.06±0.474.08±0.360.917
    AST (IU/L)21.94±8.3523.57±11.090.82024.03±10.8722.65±10.650.40723.46±8.3023.74±11.050.83827.69±9.8623.29±10.840.08822.38±6.3424.60±12.920.23723.41±9.3123.74±10.960.920
    ALT (IU/L)20.52±8.2019.28±9.430.53519.20±8.9020.33±10.390.44020.52±10.4619.60±9.380.46824.66±10.7419.20±9.23 0.018 19.20±6.6519.95±10.670.93321.29±7.5319.54±9.640.356
    Complement C3 level (mg/dL)111.98±34.98108.89±26.690.536107.30±29.44113.81±23.360.196109.45±31.33109.16±27.640.896109.06±32.70109.21±27.540.871109.36±27.59109.16±28.330.606100.26±25–26110.15±28.16 0.045
    Complement C4 level (mg/dL)22.88±15.9322.91±17.160.99622.63±18.8622.88±9.280.97020.42±9.9823.11±17.420.40722.77±9.7922.79±17.350.98224.08±20.9922.05±13.530.37121.64±10.1222.92±17.230.726
    • Data are expressed as mean and range.

    • Bold values denote statistical significance (p<0.05).

    • ALT, alanine transaminase; AST, aspartate transaminase; dsDNA, double-stranded DNA; ESR, erythrocyte sedimentation rate; Hcy, homocysteine; hs-CRP, high-sensitivity C reactive protein; RNP, ribonucleoprotein; SDI, Damage Index for Systemic Lupus Erythematosus; SLE, systemic lupus erythematosus; SLEDAI, Systemic Lupus Erythematosus Disease Activity Index; Sm, Smith; WBC, white blood cell.

  • Table 4

    Prevalence of clinical manifestations in relation to autoantibody phenotype

    Nucleosome
    (+)
    (n=31)
    Nucleosome (−)
    (n=247)
    OR (95% CI)P valuedsDNA (+) (n=204)dsDNA (−)
    (n=82)
    OR (95% CI)P valueSm (+) (n=35)Sm (−)
    (n=256)
    OR (95% CI)P valueRNP (+)
    (n=31)
    RNP (−)
    (n=261)
    OR (95% CI)P valueRo (+)
    (n=108)
    Ro (−)
    (n=184)
    OR (95% CI)P valueLa (+) (n=27)La (−) (n=265)OR (95% CI)P value
    Clinical manifestations
    Arthritis19 (65.5)129 (54.9)1.200 (0.562 to 2.562)0.638115 (56.9)39 (52.7)1.242 (0.715 to 2.158)0.44219 (57.6)136 (55.5)1.113 (0.529 to 2.344)0.77718 (62.1)137 (55.0)1.321 (0.685 to 2.547)0.40660 (57.7)95 (54.3)0.892 (0.539 to 1.477)0.65820 (80)135 (53.1)3.286 (1.184 to 9.124) 0.022
    Facial rash11 (37.9)127 (54.00.434 (0.199 to 0.946) 0.036 112 (55.4)36 (48.6)1.326 (0.759 to 2.314)0.32122 (66.7)127 (51.8)0.536 (0.246 to 1.167)0.11622 (75.9)127 (51.0)1.140 (0.474 to 2.737)0.54554 (51.9)96 (54.9)1.140 (0.688 to 1.889)0.61114 (56.0)136 (53.5)1.018 (0.439 to 2.364)0.288
    Discoid lupus3 (10.3)29 (12.3)1.313 (0.477 to 3.613)0.59822 (10.9)15 (20.3)1.866 (0.889 to 3.916)0.0995 (15.2)32 (13.1)1.203 (0.430 to 3.372)0.7254 (13.8)33 (13.3)1.473 (0.604 to 3.596)0.39512 (11.5)25 (14.3)0.793 (0.373 to 1.685)0.5464 (16.0)33 (13.0)1.277 (0.405 to 4.027)0.718
    Mucosal ulceration17 (58.6)121 (51.5)1.478 (0.698 to 3.127)0.307104 (51.5)40 (54.1)1.150 (0.664 to 1.001)0.61820 (60.6)125 (51.0)1.458 (0.692 to 3.071)0.32115 (51.7)130 (52.2)1.151 (0.795 to 1.668)0.45755 (52.9)90 (51.4)1.024 (0.623 to 1.684)0.92610 (40.0)135 (53.1)0.574 (0.246 to 1.337)0.198
    Photosensitivity20 (69.0)159 (67.7)0.720 (0.331 to 1.567)0.408129 (63.9)57 (77.0)1.829 (0.961 to 3.479)0.06624 (72.7)165 (8.6)1.286/0.557 to 2.972)0.55622 (75,9)167 (67.1)1.473 (0.604 to 3.596)0.39569 (66.3)120 (68.6)0.785 (0.456 to 1.353)0.38417 (68.0)172 (67.7)0.798 (0.326 to 1.954)0.115
    Hemolytic anemia019 (8.1%)0.000.99815 (7.4)4 (5.4)0.865 (0.268 to 2.793)0.8092 (6.1)17 (6.9)1.113 (0.242 to 5.118)0.8911 (3.4)18 (7.2)1.047 (0.684 to 1.604)0.8327 (6.7)12 (6.9)0.902 (0.335 to 2.428)0.839019 (7.5)0.000.998
    Leukopenia24 (82.8)136 (57.9)3.656 (1.354 to 9.869) 0.011 124 (61.4)41 (55.4)0.778 (0.447 to 1.354)0.37522 (66.7)146 (59.6)1.393 (0.63 to 3.019)0.40019 (65.5)149 (59.8)1.319 (0.679 to 2.560)0.41466 (63.5)102 (58.3)1.180 (0.708 to 1.966)0.52518 (72.0150 (59.1)1.734 (0.693 to 4.336)0.240
    Thrombocytopenia5 (17.2)34 (14.5)1.363 (0.496 to 3.744)0.54934 (16.8)6 (8.1)0.482 (0.188 to 1.235)0.1284 (12.1)37 (15.1)0.757 (0.244 to 2.350)4 (13.8)37 (14.9)1.115 (0.662 to 1.877)0.68312 (11.5)29 (16.6)0.752 (0.356 to 1.587)0.4554 (16)37 (14.6)1.462 (0.463 to 4.622)0.518
    Neurological3 (10.3)32 (13.6)0.630 (0.185 to 2.148)0.46025 (12.4)11 (14.9)1.036 (0.467 to 2.300)0.9306 (18.2)31 (12.7)1.589 (0.588 to 4.298)0.3624 (13.8)33 (13.3)1.211 (0.426 to 3.447)0.72012 (11.5)25 (14.3)0.657 (0.307 to 1.408)0.2801 (4.0)36 (14.2)0.231 (0.030 to 1.788)0.161
    Nephritis13 (44.8)58 (24.7)2.593 (1.169 to 5.750) 0.019 65 (32.2)8 (10.8)0.226 (0.096 to 0.531) 0.001 9 (27.3)64 (26.1)1.036 (0.436 to 2.457)0.93710 (34.5)63 (25.3)1.461 (0.626 to 3.407)0.38123 (22.1)50 (28.6)0.910 (0.499 to 1.659)0.7585 (20.0)68 (26.8)0.793 (0.276 to 2.281)0.667
    Serositis4 (13.8)27 (208)1.168 (0.392 to 3.477)0.78131 (15.3)5 (6.8)0.403 (0.148 to 1.095)0.0757 (21.2)29 (11.8)2.058 (0.815 to 5.197)0.1275 (17.2)31 (12.4)1.447 (0.514 to 4.070)0.4849 (8.7)27 (15.4)0.519 (0.231 to 1.167)0.1133 (22)33 (13.0)0.928 (0.259 to 3.325)0.908
    • Data are expressed as mean and frequency and percentage.

    • Bold values denote statistical significance (p<0.05).

    • dsDNA, double-stranded DNA; RNP, ribonucleoprotein; Sm, Smith; SSA/Ro and SSA/La, Sjogren syndrome-related antigens.

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Clinical and serological associations of autoantibodies in patients with systemic lupus erythematosus
María Correa-Rodríguez, Gabriela Pocovi-Gerardino, Jose Luis Callejas-Rubio, Raquel Ríos-Fernández, María Martín-Amada, María-Gracia Cruz-Caparrós, Blanca Rueda-Medina, Norberto Ortego-Centeno
Journal of Investigative Medicine Dec 2021, 69 (8) 1417-1425; DOI: 10.1136/jim-2021-001887

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Clinical and serological associations of autoantibodies in patients with systemic lupus erythematosus
María Correa-Rodríguez, Gabriela Pocovi-Gerardino, Jose Luis Callejas-Rubio, Raquel Ríos-Fernández, María Martín-Amada, María-Gracia Cruz-Caparrós, Blanca Rueda-Medina, Norberto Ortego-Centeno
Journal of Investigative Medicine Dec 2021, 69 (8) 1417-1425; DOI: 10.1136/jim-2021-001887
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Clinical and serological associations of autoantibodies in patients with systemic lupus erythematosus
María Correa-Rodríguez, Gabriela Pocovi-Gerardino, Jose Luis Callejas-Rubio, Raquel Ríos-Fernández, María Martín-Amada, María-Gracia Cruz-Caparrós, Blanca Rueda-Medina, Norberto Ortego-Centeno
Journal of Investigative Medicine Dec 2021, 69 (8) 1417-1425; DOI: 10.1136/jim-2021-001887
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