Skip to main content
Erschienen in: Archivum Immunologiae et Therapiae Experimentalis 1/2022

01.12.2022 | Original Article

Hydroxychloroquine Therapy and Serum Immunoglobulin Levels in Women with IgG Subclass Deficiency and Systemic Lupus Erythematosus, Sjögren Syndrome, and Rheumatoid Arthritis: A Retrospective Study

verfasst von: James C. Barton, J. Clayborn Barton, Luigi F. Bertoli

Erschienen in: Archivum Immunologiae et Therapiae Experimentalis | Ausgabe 1/2022

Einloggen, um Zugang zu erhalten

Abstract

Hydroxychloroquine (HCQ) therapy decreased immunoglobulin (Ig) levels in patients with Sjögren syndrome (SS) and rheumatoid arthritis (RA) in previous studies. We found no report of Ig levels of women with IgG subclass deficiency (IgGSD) and systemic lupus erythematosus (SLE), SS, or RA treated with HCQ. We retrospectively evaluated IgG, IgG subclass, IgA, and IgM levels and other characteristics of women at IgGSD diagnosis who did and did not take HCQ for SLE, SS, or RA. There were 132 women (48 subnormal IgG1 only, 49 combined subnormal IgG1/IgG3, and 35 subnormal IgG3 only). Mean age was 49 ± 13 years. Twenty-two women with SLE, SS, RA, or combination thereof reported HCQ ≥ 200 mg/day ≥ 6 months. In each IgGSD subtype, median Ig levels of women who took HCQ were not significantly lower than those of women who did not take HCQ. Women with combined subnormal IgG1/IgG3 who took HCQ had greater median IgG2 than women who did not take HCQ (4.89 g/L (range 4.43, 4.94) vs. 2.57 g/L (1.21, 6.44), respectively; p = 0.0123). Regressions on IgG1, IgG2, and IgG3 revealed positive associations with HCQ therapy (p = 0.0043, 0.0037, and 0.0139, respectively). There were no significant Ig associations with age, SLE, SS, or RA as independent variables. HCQ therapy of SLE, SS, or RA in women with IgGSD was not associated with significantly lower IgG, IgG subclass, IgA, or IgM levels. IgG1, IgG2, and IgG3 were positively associated with HCQ therapy, after adjustment for other variables.
Literatur
Zurück zum Zitat Armstrong RA (2014) When to use the Bonferroni correction. Ophthalmic Physiol Opt 34:502–508PubMedCrossRef Armstrong RA (2014) When to use the Bonferroni correction. Ophthalmic Physiol Opt 34:502–508PubMedCrossRef
Zurück zum Zitat Barrett DJ, Ayoub EM (1986) IgG2 subclass restriction of antibody to pneumococcal polysaccharides. Clin Exp Immunol 63:127–134PubMedPubMedCentral Barrett DJ, Ayoub EM (1986) IgG2 subclass restriction of antibody to pneumococcal polysaccharides. Clin Exp Immunol 63:127–134PubMedPubMedCentral
Zurück zum Zitat Barton JC, Bertoli LF, Barton JC (2014) Comparisons of CVID and IgGSD: referring physicians, autoimmune conditions, pneumovax reactivity, immunoglobulin levels, blood lymphocyte subsets, and HLA-A and -B typing in 432 adult index patients. J Immunol Res 2014:542706PubMedPubMedCentralCrossRef Barton JC, Bertoli LF, Barton JC (2014) Comparisons of CVID and IgGSD: referring physicians, autoimmune conditions, pneumovax reactivity, immunoglobulin levels, blood lymphocyte subsets, and HLA-A and -B typing in 432 adult index patients. J Immunol Res 2014:542706PubMedPubMedCentralCrossRef
Zurück zum Zitat Barton JC, Bertoli LF, Barton JC et al (2016) Selective subnormal IgG3 in 121 adult index patients with frequent or severe bacterial respiratory tract infections. Cell Immunol 299:50–57PubMedCrossRef Barton JC, Bertoli LF, Barton JC et al (2016) Selective subnormal IgG3 in 121 adult index patients with frequent or severe bacterial respiratory tract infections. Cell Immunol 299:50–57PubMedCrossRef
Zurück zum Zitat Barton J, Barton C, Bertoli L (2019) Duration of frequent or severe respiratory tract infection in adults before diagnosis of IgG subclass deficiency. PLoS ONE 14:e0216940PubMedPubMedCentralCrossRef Barton J, Barton C, Bertoli L (2019) Duration of frequent or severe respiratory tract infection in adults before diagnosis of IgG subclass deficiency. PLoS ONE 14:e0216940PubMedPubMedCentralCrossRef
Zurück zum Zitat Barton JC, Barton JC, Bertoli LF (2022) Hydroxychloroquine therapy and other observations in 132 women with three common IgGSD subtypes. Open Science Framework https://osf.io/hbfdc/. Accessed 02 may 2022 Barton JC, Barton JC, Bertoli LF (2022) Hydroxychloroquine therapy and other observations in 132 women with three common IgGSD subtypes. Open Science Framework https://​osf.​io/​hbfdc/​. Accessed 02 may 2022
Zurück zum Zitat Barton JC, Barton JC, Bertoli LF et al (2020a) Characterization of adult patients with IgG subclass deficiency and subnormal IgG2. PLoS ONE 15:e0240522PubMedPubMedCentralCrossRef Barton JC, Barton JC, Bertoli LF et al (2020a) Characterization of adult patients with IgG subclass deficiency and subnormal IgG2. PLoS ONE 15:e0240522PubMedPubMedCentralCrossRef
Zurück zum Zitat Barton JC, Barton JC, Bertoli LF et al (2020b) HLA-A and -B type and haplotype frequencies in IgG subclass deficiency subgroups. Arch Immunol Ther Exp 68:14CrossRef Barton JC, Barton JC, Bertoli LF et al (2020b) HLA-A and -B type and haplotype frequencies in IgG subclass deficiency subgroups. Arch Immunol Ther Exp 68:14CrossRef
Zurück zum Zitat Blanco F, Kalsi J, Ravirajan CT et al (1992) IgG subclasses in systemic lupus erythematosus and other autoimmune rheumatic diseases. Lupus 1:391–399PubMedCrossRef Blanco F, Kalsi J, Ravirajan CT et al (1992) IgG subclasses in systemic lupus erythematosus and other autoimmune rheumatic diseases. Lupus 1:391–399PubMedCrossRef
Zurück zum Zitat Bodewes ILA, Gottenberg JE, van Helden-Meeuwsen CG et al (2020) Hydroxychloroquine treatment downregulates systemic interferon activation in primary Sjögren’s syndrome in the JOQUER randomized trial. Rheumatology 59:107–111PubMedCrossRef Bodewes ILA, Gottenberg JE, van Helden-Meeuwsen CG et al (2020) Hydroxychloroquine treatment downregulates systemic interferon activation in primary Sjögren’s syndrome in the JOQUER randomized trial. Rheumatology 59:107–111PubMedCrossRef
Zurück zum Zitat Bousfiha A, Jeddane L, Picard C et al (2018) The 2017 IUIS phenotypic classification for primary immunodeficiencies. J Clin Immunol 38:129–143PubMedCrossRef Bousfiha A, Jeddane L, Picard C et al (2018) The 2017 IUIS phenotypic classification for primary immunodeficiencies. J Clin Immunol 38:129–143PubMedCrossRef
Zurück zum Zitat Crisp HC, Quinn JM (2019) Quantitative immunoglobulins in adulthood. Allergy Asthma Proc 30:649–654CrossRef Crisp HC, Quinn JM (2019) Quantitative immunoglobulins in adulthood. Allergy Asthma Proc 30:649–654CrossRef
Zurück zum Zitat de la Torre MC, Toran P, Serra-Prat M et al (2016) Serum levels of immunoglobulins and severity of community-acquired pneumonia. BMJ Open Respir Res 3:e000152PubMedPubMedCentralCrossRef de la Torre MC, Toran P, Serra-Prat M et al (2016) Serum levels of immunoglobulins and severity of community-acquired pneumonia. BMJ Open Respir Res 3:e000152PubMedPubMedCentralCrossRef
Zurück zum Zitat Eriksson P, Andersson C, Ekerfelt C et al (2004) Relationship between serum levels of IL-18 and IgG1 in patients with primary Sjogren’s syndrome, rheumatoid arthritis and healthy controls. Clin Exp Immunol 137:617–620PubMedPubMedCentralCrossRef Eriksson P, Andersson C, Ekerfelt C et al (2004) Relationship between serum levels of IL-18 and IgG1 in patients with primary Sjogren’s syndrome, rheumatoid arthritis and healthy controls. Clin Exp Immunol 137:617–620PubMedPubMedCentralCrossRef
Zurück zum Zitat Fauchais AL, Ouattara B, Gondran G et al (2010) Articular manifestations in primary Sjögren’s syndrome: clinical significance and prognosis of 188 patients. Rheumatology 49:1164–1172PubMedCrossRef Fauchais AL, Ouattara B, Gondran G et al (2010) Articular manifestations in primary Sjögren’s syndrome: clinical significance and prognosis of 188 patients. Rheumatology 49:1164–1172PubMedCrossRef
Zurück zum Zitat Fox RI, Chan E, Benton L et al (1988) Treatment of primary Sjögren’s syndrome with hydroxychloroquine. Am J Med 85:62–67PubMedCrossRef Fox RI, Chan E, Benton L et al (1988) Treatment of primary Sjögren’s syndrome with hydroxychloroquine. Am J Med 85:62–67PubMedCrossRef
Zurück zum Zitat Gabay C, Bel M, Combescure C et al (2011) Impact of synthetic and biologic disease-modifying antirheumatic drugs on antibody responses to the AS03-adjuvanted pandemic influenza vaccine: a prospective, open-label, parallel-cohort, single-center study. Arthritis Rheum 63:1486–1496PubMedCrossRef Gabay C, Bel M, Combescure C et al (2011) Impact of synthetic and biologic disease-modifying antirheumatic drugs on antibody responses to the AS03-adjuvanted pandemic influenza vaccine: a prospective, open-label, parallel-cohort, single-center study. Arthritis Rheum 63:1486–1496PubMedCrossRef
Zurück zum Zitat Gibbs JG, Pratt EL, Fisher LH et al (2006) Recurrent pneumonia associated with hydroxychloroquine. J Allergy Clin Immunol 117:S170–S171CrossRef Gibbs JG, Pratt EL, Fisher LH et al (2006) Recurrent pneumonia associated with hydroxychloroquine. J Allergy Clin Immunol 117:S170–S171CrossRef
Zurück zum Zitat Gonzalez-Quintela A, Alende R, Gude F et al (2008) Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin Exp Immunol 151:42–50PubMedPubMedCentralCrossRef Gonzalez-Quintela A, Alende R, Gude F et al (2008) Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin Exp Immunol 151:42–50PubMedPubMedCentralCrossRef
Zurück zum Zitat Grönwall C, Hardt U, Gustafsson JT et al (2017) Depressed serum IgM levels in SLE are restricted to defined subgroups. Clin Immunol 183:304–315PubMedCrossRef Grönwall C, Hardt U, Gustafsson JT et al (2017) Depressed serum IgM levels in SLE are restricted to defined subgroups. Clin Immunol 183:304–315PubMedCrossRef
Zurück zum Zitat Hammarström L, Vorechovsky I, Webster D (2000) Selective IgA deficiency (SIgAD) and common variable immunodeficiency (CVID). Clin Exp Immunol 120:225–231PubMedPubMedCentralCrossRef Hammarström L, Vorechovsky I, Webster D (2000) Selective IgA deficiency (SIgAD) and common variable immunodeficiency (CVID). Clin Exp Immunol 120:225–231PubMedPubMedCentralCrossRef
Zurück zum Zitat Khokar A, Gupta S (2019) Clinical and immunological features of 78 adult patients with primary selective IgG subclass deficiencies. Arch Immunol Ther Exp 67:325–334CrossRef Khokar A, Gupta S (2019) Clinical and immunological features of 78 adult patients with primary selective IgG subclass deficiencies. Arch Immunol Ther Exp 67:325–334CrossRef
Zurück zum Zitat Kim JH, Park S, Hwang YI et al (2016) Immunoglobulin G subclass deficiencies in adult patients with chronic airway diseases. J Korean Med Sci 31:1560–1565PubMedPubMedCentralCrossRef Kim JH, Park S, Hwang YI et al (2016) Immunoglobulin G subclass deficiencies in adult patients with chronic airway diseases. J Korean Med Sci 31:1560–1565PubMedPubMedCentralCrossRef
Zurück zum Zitat Knight AK, Cunningham-Rundles C (2005) Oxcarbazepine-induced immunoglobulin deficiency. Clin Diagn Lab Immunol 12:560–561PubMedPubMedCentral Knight AK, Cunningham-Rundles C (2005) Oxcarbazepine-induced immunoglobulin deficiency. Clin Diagn Lab Immunol 12:560–561PubMedPubMedCentral
Zurück zum Zitat Lacombe C, Aucouturier P, Preud’homme JL (1997) Selective IgG1 deficiency. Clin Immunol Immunopathol 84:194–201PubMedCrossRef Lacombe C, Aucouturier P, Preud’homme JL (1997) Selective IgG1 deficiency. Clin Immunol Immunopathol 84:194–201PubMedCrossRef
Zurück zum Zitat Lin GG, Li JM (2009) IgG subclass serum levels in systemic lupus erythematosus patients. Clin Rheumatol 28:1315–1318PubMedCrossRef Lin GG, Li JM (2009) IgG subclass serum levels in systemic lupus erythematosus patients. Clin Rheumatol 28:1315–1318PubMedCrossRef
Zurück zum Zitat Lin G, Li J (2010) Elevation of serum IgG subclass concentration in patients with rheumatoid arthritis. Rheumatol Int 30:837–840PubMedCrossRef Lin G, Li J (2010) Elevation of serum IgG subclass concentration in patients with rheumatoid arthritis. Rheumatol Int 30:837–840PubMedCrossRef
Zurück zum Zitat Mantovani AP, Monclaro MP, Skare TL (2010) Prevalence of IgA deficiency in adult systemic lupus erythematosus and the study of the association with its clinical and autoantibody profiles. Rev Bras Reumatol 50:273–282PubMedCrossRef Mantovani AP, Monclaro MP, Skare TL (2010) Prevalence of IgA deficiency in adult systemic lupus erythematosus and the study of the association with its clinical and autoantibody profiles. Rev Bras Reumatol 50:273–282PubMedCrossRef
Zurück zum Zitat Parker AR, Skold M, Harding S et al (2019) Pneumococcal vaccination responses in adults with subnormal IgG subclass concentrations. BMC Immunol 20:29PubMedPubMedCentralCrossRef Parker AR, Skold M, Harding S et al (2019) Pneumococcal vaccination responses in adults with subnormal IgG subclass concentrations. BMC Immunol 20:29PubMedPubMedCentralCrossRef
Zurück zum Zitat Pavelka K Jr, Sen KP, Peliskova Z et al (1989) Hydroxychloroquine sulphate in the treatment of rheumatoid arthritis: a double blind comparison of two dose regimens. Ann Rheum Dis 48:542–546PubMedPubMedCentralCrossRef Pavelka K Jr, Sen KP, Peliskova Z et al (1989) Hydroxychloroquine sulphate in the treatment of rheumatoid arthritis: a double blind comparison of two dose regimens. Ann Rheum Dis 48:542–546PubMedPubMedCentralCrossRef
Zurück zum Zitat Pelka K, Matyja-Bednarczyk A, Wojas-Pelc A et al (2021) Hydroxychloroquine does not impair antibody response to 13-valent pneumococcal conjugate vaccine in patients with cutaneous lupus erythematosus-A pilot study. Dermatol Ther 34:e15013PubMedCrossRef Pelka K, Matyja-Bednarczyk A, Wojas-Pelc A et al (2021) Hydroxychloroquine does not impair antibody response to 13-valent pneumococcal conjugate vaccine in patients with cutaneous lupus erythematosus-A pilot study. Dermatol Ther 34:e15013PubMedCrossRef
Zurück zum Zitat Schauer U, Stemberg F, Rieger CH et al (2003) Levels of antibodies specific to tetanus toxoid, Haemophilus influenzae type b, and pneumococcal capsular polysaccharide in healthy children and adults. Clin Diagn Lab Immunol 10:202–207PubMedPubMedCentral Schauer U, Stemberg F, Rieger CH et al (2003) Levels of antibodies specific to tetanus toxoid, Haemophilus influenzae type b, and pneumococcal capsular polysaccharide in healthy children and adults. Clin Diagn Lab Immunol 10:202–207PubMedPubMedCentral
Zurück zum Zitat Siber GR, Schur PH, Aisenberg AC et al (1980) Correlation between serum IgG-2 concentrations and the antibody response to bacterial polysaccharide antigens. N Engl J Med 303:178–182PubMedCrossRef Siber GR, Schur PH, Aisenberg AC et al (1980) Correlation between serum IgG-2 concentrations and the antibody response to bacterial polysaccharide antigens. N Engl J Med 303:178–182PubMedCrossRef
Zurück zum Zitat Söderström T, Söderström R, Avanzini A et al (1987) Immunoglobulin G subclass deficiencies. Int Arch Allergy Immunol 82:476–480CrossRef Söderström T, Söderström R, Avanzini A et al (1987) Immunoglobulin G subclass deficiencies. Int Arch Allergy Immunol 82:476–480CrossRef
Zurück zum Zitat van der Heijden EH, Hartgring SA, Kruize AA et al (2019) Additive immunosuppressive effect of leflunomide and hydroxychloroquine supports rationale for combination therapy for Sjögren’s syndrome. Expert Rev Clin Immunol 15:801–808PubMedCrossRef van der Heijden EH, Hartgring SA, Kruize AA et al (2019) Additive immunosuppressive effect of leflunomide and hydroxychloroquine supports rationale for combination therapy for Sjögren’s syndrome. Expert Rev Clin Immunol 15:801–808PubMedCrossRef
Zurück zum Zitat Van Kessel DA, Horikx PE, Van Houte AJ et al (1999) Clinical and immunological evaluation of patients with mild IgG1 deficiency. Clin Exp Immunol 118:102–107PubMedPubMedCentralCrossRef Van Kessel DA, Horikx PE, Van Houte AJ et al (1999) Clinical and immunological evaluation of patients with mild IgG1 deficiency. Clin Exp Immunol 118:102–107PubMedPubMedCentralCrossRef
Zurück zum Zitat Veys EM, Gabriel PA, Coigne E et al (1976) Rheumatoid factor and serum IgG, IgM and IgA levels in rheumatoid arthritis with vasculitis. Scand J Rheumatol 5:1–6PubMed Veys EM, Gabriel PA, Coigne E et al (1976) Rheumatoid factor and serum IgG, IgM and IgA levels in rheumatoid arthritis with vasculitis. Scand J Rheumatol 5:1–6PubMed
Zurück zum Zitat World Medical Association (2013) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310:2191–2194CrossRef World Medical Association (2013) World Medical Association Declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA 310:2191–2194CrossRef
Metadaten
Titel
Hydroxychloroquine Therapy and Serum Immunoglobulin Levels in Women with IgG Subclass Deficiency and Systemic Lupus Erythematosus, Sjögren Syndrome, and Rheumatoid Arthritis: A Retrospective Study
verfasst von
James C. Barton
J. Clayborn Barton
Luigi F. Bertoli
Publikationsdatum
01.12.2022
Verlag
Springer International Publishing
Erschienen in
Archivum Immunologiae et Therapiae Experimentalis / Ausgabe 1/2022
Print ISSN: 0004-069X
Elektronische ISSN: 1661-4917
DOI
https://doi.org/10.1007/s00005-022-00652-x

Weitere Artikel der Ausgabe 1/2022

Archivum Immunologiae et Therapiae Experimentalis 1/2022 Zur Ausgabe