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Research ArticleSystemic Lupus Erythematosus

Predictors of Remission and Low Disease Activity State in Systemic Lupus Erythematosus: Data from a Multiethnic, Multinational Latin American Cohort

Manuel F. Ugarte-Gil, Daniel Wojdyla, Guillermo J. Pons-Estel, Rosana Quintana, José A. Gómez-Puerta, Luis J. Catoggio, Alejandro Alvarellos, Verónica Saurit, Eduardo Borba, Emilia Sato, Lilian Costallat, Nilzio A. Da Silva, Antonio Iglesias-Gamarra, Oscar Neira, Gil Reyes-Llerena, Mario H. Cardiel, Mary Carmen Amigo, Eduardo Acevedo-Vásquez, María H. Esteva-Spinetti, Graciela S. Alarcón and Bernardo A. Pons-Estel
The Journal of Rheumatology October 2019, 46 (10) 1299-1308; DOI: https://doi.org/10.3899/jrheum.180433
Manuel F. Ugarte-Gil
From the Department of Rheumatology, Hospital Guillermo Almenara Irigoyen, EsSalud; Universidad Científica del Sur, Lima, Peru; Grupo Latino Americano De Estudio de Lupus (GLADEL), Rosario, Argentina; Department of Autoimmune Diseases, Hospital Clinic, Barcelona, Spain; Centro Regional de Enfermedades Autoinmunes y Reumáticas (CREAR), Grupo Oroño, Sanatorio Parque, Rosario, Santa Fe, Argentina; Servicio de Reumatología, Hospital Clinic, Barcelona, Spain; Sección de Reumatología, Servicio de Clínica Médica, Hospital Italiano de Buenos Aires, Instituto Universitario, Escuela de Medicina Hospital Italiano and Fundación Dr. Pedro M. Catoggio para el Progreso de la Reumatología, Buenos Aires; Servicio de Reumatología, Hospital Privado, Centro Medico de Córdoba, Córdoba, Argentina; Rheumatology Division, Hospital das Clínicas HCFMUSP, Faculdade de Medicina, Universidade de São Paulo; Disciplina de Reumatologia, Escola Paulista de Medicina/UNIFESP, Hospital São Paulo, Universidade Federal de São Paulo, São Paulo; Faculdade de Ciências Médicas, Universidade Estadual de Campinas, Campinas; Faculdade de Medicina, Universidade Federal de Goiás, Goiânia, Brazil; Clínica Saludcoop 104 Jorge Piñeros Corpas and Hospital San Juan de Dios, Universidad Nacional de Colombia, Bogotá, Colombia; Hospital del Salvador, Facultad de Medicina, Universidad de Chile, Santiago, Chile; Servicio de Reumatología, Centro de Investigaciones Médico Quirúrgicas-CIMEQ, Havana, Cuba; Centro de Investigación Clínica de Morelia SC, Morelia, Michoacán; Reumatología, Centro Médico ABC, Ciudad de México, México; Universidad Nacional Mayor de San Marcos, Lima, Peru; Hospital Central de San Cristóbal, San Cristóbal, Venezuela; Department of Medicine, Division of Clinical Immunology and Rheumatology, School of Medicine, University of Alabama at Birmingham, Birmingham, Alabama, USA.
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  • For correspondence: manuel_ugarte@yahoo.com
Daniel Wojdyla
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Guillermo J. Pons-Estel
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Rosana Quintana
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José A. Gómez-Puerta
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Luis J. Catoggio
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Alejandro Alvarellos
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Verónica Saurit
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Eduardo Borba
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Emilia Sato
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Lilian Costallat
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Nilzio A. Da Silva
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Antonio Iglesias-Gamarra
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Oscar Neira
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Gil Reyes-Llerena
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Mario H. Cardiel
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Mary Carmen Amigo
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Eduardo Acevedo-Vásquez
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María H. Esteva-Spinetti
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Graciela S. Alarcón
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Bernardo A. Pons-Estel
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    Figure 1.

    Predictors of remission in the GLADEL cohort. A. Presence of mucocutaneous involvement. B. Presence of hematologic involvement. C. Presence of renal involvement. D. Use of immunosuppressive drugs. E. SLEDAI at baseline (categorized). SLEDAI: Systemic Lupus Erythematosus Disease Activity Index.

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    Table 1.

    Characteristics of patients with systemic lupus erythematosus (SLE) in this study.

    CharacteristicOverall, n = 902
    Sociodemographic
    Sex
      Male93 (10.3)
      Female809 (89.7)
    Age at diagnosis, yrs26, 20–36
    Age at first symptom, yrs25, 19–34
    Age at entry, yrs27, 20–36
    Race or ethnic group
      White368 (40.9)
      Mestizo378 (42.0)
      African Latin American121 (13.5)
      Other32 (3.6)
    Socioeconomic status
      High/middle high81 (9.0)
      Middle253 (28.1)
      Middle low/low565 (62.8)
    Residence
      Urban817 (91.1)
      Rural80 (8.9)
    Medical coverage
      None135 (15.0)
      Partial227 (25.3)
      Full536 (59.7)
    Education, yrs
      0–7264 (30.5)
      8–12400 (46.2)
      ≥ 13202 (23.3)
    Disease duration at entry, mos
      Entered at diagnosis545 (60.4)
      Up to 6132 (14.6)
      6 to 12101 (11.2)
      13 to 24124 (13.7)
    Clinical characteristics at entry
    General manifestations652 (72.3)
    Musculoskeletal813 (90.1)
    Mucocutaneous800 (88.7)
    Ocular82 (9.1)
    Lung40 (4.4)
    Cardiovascular298 (33.0)
    Renal398 (44.1)
    Neurological181 (20.1)
    Hematological609 (67.5)
    Immunological583/725 (80.4)
    Treatments at entry
    Antimalarials279 (30.9)
    Prednisone (higher dose before baseline)
      None427 (47.3)
      Low (≤ 7.5 mg/day)16 (1.8)
      Medium (> 7.5 ≤ 15 mg/day)83 (9.2)
      High (> 15 < 60 mg/day)256 (28.4)
      Very high (≥ 60 mg/day)120 (13.3)
    Immunosuppressive drugs166 (18.4)
    Disease status (SLEDAI) at entry10, 6–16
    • Data are n (%) or median, 25th–75th percentiles. SLEDAI: Systemic Lupus Erythematosus Disease Activity Index.

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    Table 2.

    Variables associated with remission by univariable analyses.

    CharacteristicRemission During Followup
    Yes (n = 196), n (%) or median (25th–75th percentiles)No (n = 706), n (%) or median (25th–75th percentiles)p
    Sociodemographic
    Sex0.4454
      Male18 (9.2)75 (10.6)
      Female178 (90.8)631 (89.4)
    Age at diagnosis, yrs28, 21–3926, 20–350.0809
    Age at first symptom, yrs27, 19–3725, 19–340.1806
    Age at entry, yrs28, 21–4026, 20–350.0644
    Race or ethnic group0.9977
      White86 (43.9)282 (40.1)
      Mestizo80 (40.8)298 (42.4)
      African Latin American25 (12.8)96 (13.7)
      Other5 (2.6)27 (3.8)
    Socioeconomic status0.0030
      High/middle high27 (13.9)54 (7.7)
      Middle63 (32.5)190 (27.0)
      Middle low/low104 (53.6)461 (65.4)
    Residence0.0605
      Urban185 (94.9)632 (90.0)
      Rural10 (5.1)70 (10.0)
    Medical coverage0.0676
      None17 (8.7)118 (16.8)
      Partial55 (28.2)172 (24.5)
      Full123 (63.1)413 (58.7)
    Education, yrs0.0095
      0–750 (25.9)214 (31.8)
      8–1287 (45.1)313 (46.5)
      ≥ 1356 (29.0)146 (21.7)
    Disease duration at entry, mos0.1454
      Entered at diagnosis107 (54.6)438 (62.0)
      Up to 624 (12.2)108 (15.3)
      6 to 1226 (13.3)75 (10.6)
      13 to 2439 (19.9)85 (12.0)
    Clinical characteristics at entry
    General manifestations135 (68.9)517 (73.2)0.0742
    Musculoskeletal183 (93.4)630 (89.2)0.5158
    Mucocutaneous165 (84.2)635 (89.9)0.0490
    Ocular21 (10.7)61 (8.6)0.6735
    Lung7 (3.6)33 (4.7)0.3088
    Cardiovascular60 (30.6)238 (33.7)0.5569
    Renal68 (34.7)330 (46.7)0.0085
    Neurological35 (17.9)146 (20.7)0.4796
    Hematological122 (62.2)487 (69.0)0.0655
    Immunological123/157 (78.3)460/568 (81.0)0.3216
    Treatments at entry
    Antimalarials69 (35.2)210 (29.7)0.3478
    Prednisone (higher dose before baseline)0.1604
      None86 (43.9)341 (48.3)
      Low (≤ 7.5 mg/day)5 (2.6)11 (1.6)
      Medium (> 7.5 ≤ 15 mg/day)21 (10.7)62 (8.8)
      High (> 15 < 60 mg/day)50 (25.5)206 (29.2)
      Very high (≥ 60 mg/day)34 (17.3)86 (12.2)
    Immunosuppressive drugs46 (23.5)120 (17.0)0.1139
    Disease status (SLEDAI) at entry8, 5–1310, 6–170.0002
    • Data are n (%) or median, 25th–75th percentiles. SLEDAI: Systemic Lupus Erythematosus Disease Activity Index.

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    Table 3.

    Variables associated with low disease activity state (LDAS) by univariable analyses.

    CharacteristicLDAS During Followup
    Yes (n = 314), n (%) or median (25th–75th percentiles)No (n = 588), n (%) or median (25th–75th percentiles)p
    Sociodemographic
    Sex0.4250
      Male30 (9.6)63 (10.7)
      Female284 (90.4)525 (89.3)
    Age at diagnosis, yrs28, 21–3925, 19–340.0024
    Age at first symptom, yrs27, 19–3724, 18–330.0095
    Age at entry, yrs28, 21–3926, 20–340.0020
    Ethnic group0.8450
      White141 (44.9)227 (38.8)
      Mestizo129 (41.1)249 (42.6)
      African Latin American37 (11.8)84 (14.4)
      Other7 (2.2)25 (4.3)
    Socioeconomic status0.0099
      High/middle high39 (12.5)42 (7.1)
      Middle97 (31.2)156 (26.5)
      Middle low/low175 (56.3)390 (66.3)
    Residence0.1767
      Urban291 (93.0)526 (90.1)
      Rural22 (7.0)58 (9.9)
    Medical coverage0.3530
      None36 (11.5)99 (16.9)
      Partial83 (26.5)144 (24.6)
      Full194 (62.0)342 (58.5)
    Education, yrs0.0073
      0–786 (27.9)178 (31.9)
      8–12134 (43.5)266 (47.7)
      ≥ 1388 (28.6)114 (20.4)
    Disease duration at entry, mos0.4751
      Entered at diagnosis178 (56.7)367 (62.4)
      Up to 647 (15.0)85 (14.5)
      6 to 1238 (12.1)63 (10.7)
      13 to 2451 (16.2)73 (12.4)
    Clinical characteristics at entry
    General manifestations216 (68.8)436 (74.1)0.0065
    Musculoskeletal294 (93.6)519 (88.3)0.2147
    Mucocutaneous269 (85.7)531 (90.3)0.0365
    Ocular35 (11.1)47 (8.0)0.2817
    Lung10 (3.2)30 (5.1)0.0611
    Cardiovascular89 (28.3)209 (35.5)0.0682
    Renal108 (34.4)290 (49.3)0.0003
    Neurological56 (17.8)125 (21.3)0.4050
    Hematological204 (65.0)405 (68.9)0.2707
    Immunological197/251 (78.5)386/474 (81.4)0.2052
    Treatments at entry
    Antimalarials108 (34.4)171 (29.1)0.2091
    Prednisone (higher dose before baseline)0.0252
      None139 (44.3)288 (49.0)
      Low (≤ 7.5 mg/day)7 (2.2)9 (1.5)
      Medium (> 7.5 ≤ 15 mg/day)40 (12.7)43 (7.3)
      High (> 15 < 60 mg/day)84 (26.8)172 (29.3)
      Very high (≥ 60 mg/day)44 (14.0)76 (12.9)
    Immunosuppressive drugs65 (20.7)101 (17.2)0.3585
    Disease status (SLEDAI) at entry8, 5–1311, 6–17< 0.0001
    • Data are n (%) or median, 25th–75th percentiles. SLEDAI: Systemic Lupus Erythematosus Disease Activity Index.

    • View popup
    Table 4.

    Predictors of remission; multivariable model.

    PredictorHR (95% CI)p
    Medical coverage
      None0.628 (0.375–1.052)0.0774
      Partial1.257 (0.908–1.740)0.1675
      FullRef
    Absence of mucocutaneous manifestations*1.571 (1.064–2.320)0.0230
    Absence of renal involvement*1.487 (1.067–2.073)0.0191
    Absence of hematologic involvement*1.354 (1.005–1.825)0.0463
    Immunosuppressive drug use1.468 (1.025–2.105)0.0364
    SLEDAI at entry, per 1-unit decrease1.028 (1.006–1.051)0.0112
    • ↵* Before or at cohort entry. SLEDAI: Systemic Lupus Erythematosus Disease Activity Index.

    • View popup
    Table 5.

    Predictors of low disease activity state; multivariable model.

    PredictorHR (95% CI)p
    Age at cohort entry, per 5-yr increase1.050 (1.004–1.098)0.0341
    Absence of mucocutaneous manifestations*1.401 (1.016–1.930)0.0394
    Absence of renal involvement*1.344 (1.049–1.721)0.0194
    SLEDAI at cohort entry, per 1-unit decrease1.025 (1.009–1.042)0.0027
    • ↵* Before or at cohort entry. SLEDAI: Systemic Lupus Erythematosus Disease Activity Index.

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Predictors of Remission and Low Disease Activity State in Systemic Lupus Erythematosus: Data from a Multiethnic, Multinational Latin American Cohort
Manuel F. Ugarte-Gil, Daniel Wojdyla, Guillermo J. Pons-Estel, Rosana Quintana, José A. Gómez-Puerta, Luis J. Catoggio, Alejandro Alvarellos, Verónica Saurit, Eduardo Borba, Emilia Sato, Lilian Costallat, Nilzio A. Da Silva, Antonio Iglesias-Gamarra, Oscar Neira, Gil Reyes-Llerena, Mario H. Cardiel, Mary Carmen Amigo, Eduardo Acevedo-Vásquez, María H. Esteva-Spinetti, Graciela S. Alarcón, Bernardo A. Pons-Estel
The Journal of Rheumatology Oct 2019, 46 (10) 1299-1308; DOI: 10.3899/jrheum.180433

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Predictors of Remission and Low Disease Activity State in Systemic Lupus Erythematosus: Data from a Multiethnic, Multinational Latin American Cohort
Manuel F. Ugarte-Gil, Daniel Wojdyla, Guillermo J. Pons-Estel, Rosana Quintana, José A. Gómez-Puerta, Luis J. Catoggio, Alejandro Alvarellos, Verónica Saurit, Eduardo Borba, Emilia Sato, Lilian Costallat, Nilzio A. Da Silva, Antonio Iglesias-Gamarra, Oscar Neira, Gil Reyes-Llerena, Mario H. Cardiel, Mary Carmen Amigo, Eduardo Acevedo-Vásquez, María H. Esteva-Spinetti, Graciela S. Alarcón, Bernardo A. Pons-Estel
The Journal of Rheumatology Oct 2019, 46 (10) 1299-1308; DOI: 10.3899/jrheum.180433
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Keywords

SYSTEMIC LUPUS ERYTHEMATOSUS
REMISSION
LOW DISEASE ACTIVITY STATE
RISK FACTORS

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