Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on medication adherence

LIVE: Thursday 27th June 2024, 18:00-19:30 (CEST)
Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.
ADVANCED SEARCH
Log in
Top
Allergy, Asthma & Clinical Immunology
Published in: Allergy, Asthma & Clinical Immunology 1/2020

01-12-2020 | Systemic Lupus Erythematosus | Research

Co-occurrence between C1 esterase inhibitor deficiency and autoimmune disease: a systematic literature review

Authors: Donald Levy, Timothy Craig, Paul K. Keith, Girishanthy Krishnarajah, Rachel Beckerman, Subhransu Prusty

Published in: Allergy, Asthma & Clinical Immunology | Issue 1/2020

Login to get access

Abstract

Background

Hereditary angioedema (HAE) is caused by a SERPING1 gene defect resulting in decreased (Type I) or dysfunctional (Type II) C1 esterase inhibitor (C1-INH). The prevalence of autoimmune diseases (ADs) in patients with HAE appears to be higher than the general population. A systematic literature review was conducted to examine the co-occurrence between HAE and ADs.

Methods

PubMed/EMBASE were searched for English-language reviews, case reports, observational studies, retrospective studies, and randomized controlled trials up to 04/15/2018 (04/15/2015-04/15/2018 for EMBASE) that mentioned patients with HAE Type I or II and comorbid ADs. Non-human or in vitro studies and publications of C1-INH deficiency secondary to lymphoproliferative disorders or angiotensin-converting-enzyme inhibitors were excluded.

Results

Of the 2880 records screened, 76 met the eligibility criteria and 155 individual occurrences of co-occurring HAE and AD were mentioned. The most common ADs were systemic lupus erythematosus (30 mentions), thyroid disease (21 mentions), and glomerulonephritis (16 mentions). When ADs were grouped by MedDRA v21.0 High Level Terms, the most common were: Lupus Erythematosus and Associated Conditions, n = 52; Endocrine Autoimmune Disorders, n = 21; Gastrointestinal Inflammatory Conditions, n = 16; Glomerulonephritis and Nephrotic Syndrome, n = 16; Rheumatoid Arthritis and Associated Conditions, n = 11; Eye, Salivary Gland and Connective Tissue Disorders, n = 10; and Immune and Associated Conditions Not Elsewhere Classified, n = 5.

Conclusions

Based on literature reports, systemic lupus erythematosus is the most common AD co-occurring with HAE Type I and II. Cause and effect for co-occurring HAE and AD has not been clinically established but could be related to lack of sufficient C1-INH function.
Literature
1.
Davis AE 3rd, Lu F, Mejia P. C1 inhibitor, a multi-functional serine protease inhibitor. Thromb Haemost. 2010;104(5):886–93.PubMed
2.
Steiner UC, Keller M, Schmid P, Cichon S, Wuillemin WA. Mutational spectrum of the SERPING1 gene in Swiss patients with hereditary angioedema. Clin Exp Immunol. 2017;188(3):430–6.PubMedPubMedCentralCrossRef
3.
Johnsrud I, Kulseth MA, Rodningen OK, Landro L, Helsing P, Waage Nielsen E, et al. A nationwide study of Norwegian patients with hereditary angioedema with C1 inhibitor deficiency identified six novel mutations in SERPING1. PLoS ONE. 2015;10(7):e0131637.PubMedPubMedCentralCrossRef
4.
Agostoni A, Aygoren-Pursun E, Binkley KE, Blanch A, Bork K, Bouillet L, et al. Hereditary and acquired angioedema: problems and progress: proceedings of the third C1 esterase inhibitor deficiency workshop and beyond. J Allergy Clin Immunol. 2004;114(3 Suppl):S51–131.PubMedPubMedCentralCrossRef
5.
Nussberger J, Cugno M, Cicardi M. Bradykinin-mediated angioedema. N Engl J Med. 2002;347(8):621–2.PubMedCrossRef
6.
Betschel S, Badiou J, Binkley K, Hebert J, Kanani A, Keith P, et al. Canadian hereditary angioedema guideline. Allergy Asthma Clin Immunol. 2014;10(1):50.PubMedPubMedCentralCrossRef
7.
Craig T, Aygoren-Pursun E, Bork K, Bowen T, Boysen H, Farkas H, et al. WAO guideline for the management of hereditary angioedema. World Allergy Organ J. 2012;5(12):182–99.PubMedPubMedCentralCrossRef
8.
Longhurst HJ, Tarzi MD, Ashworth F, Bethune C, Cale C, Dempster J, et al. C1 inhibitor deficiency: 2014 United Kingdom consensus document. Clin Exp Immunol. 2015;180(3):475–83.PubMedPubMedCentralCrossRef
9.
Maurer M, Magerl M, Ansotegui I, Aygoren-Pursun E, Betschel S, Bork K, et al. The international WAO/EAACI guideline for the management of hereditary angioedema-The 2017 revision and update. Allergy. 2018;73(8):1575–96.PubMedCrossRef
10.
Takhzyro™ (lanadelumab-flyo). Full prescribing information. Lexington, MA: Shire; 2018.
11.
Lintner KE, Wu YL, Yang Y, Spencer CH, Hauptmann G, Hebert LA, et al. Early components of the complement classical activation pathway in human systemic autoimmune diseases. Front Immunol. 2016;7:36.PubMedPubMedCentralCrossRef
12.
13.
Kaplan AP. Enzymatic pathways in the pathogenesis of hereditary angioedema: the role of C1 inhibitor therapy. J Allergy Clin Immunol. 2010;126(5):918–25.PubMedCrossRef
14.
Triggianese P, Guarino MD, Ballanti E, Chimenti MS, Perricone R. Hereditary angioedema and autoimmunity. Isr Med Assoc J. 2014;16(10):622–4.PubMed
15.
16.
Fischer MB, Ma M, Goerg S, Zhou X, Xia J, Finco O, et al. Regulation of the B cell response to T-dependent antigens by classical pathway complement. J Immunol. 1996;157(2):549–56.PubMed
17.
Truedsson L, Bengtsson AA, Sturfelt G. Complement deficiencies and systemic lupus erythematosus. Autoimmunity. 2007;40(8):560–6.PubMedCrossRef
18.
Tsokos GC, Lo MS, Costa Reis P, Sullivan KE. New insights into the immunopathogenesis of systemic lupus erythematosus. Nat Rev Rheumatol. 2016;12(12):716–30.CrossRefPubMed
19.
D’Amelio R, Perricone R, De Carolis C, Pontesilli O, Matricardi PM, Fontana L. Immune complexes in hereditary angioneurotic edema (HANE). J Allergy Clin Immunol. 1986;78(3 Pt 1):486–7.PubMedCrossRef
20.
Donaldson VH, Hess EV, McAdams AJ. Lupus-erythematosus-like disease in three unrelated women with hereditary angioneurotic edema. Ann Intern Med. 1977;86(3):312–3.PubMedCrossRef
21.
Gallais Sérézal I, Bouillet L, Dhôte R, Gayet S, Jeandel PY, Blanchard-Delaunay C, et al. Hereditary angioedema and lupus: a French retrospective study and literature review. Autoimmun Rev. 2015;14(6):564–8.PubMedCrossRef
22.
Hory B, Haultier JJ. Glomerulonephritis and hereditary angioedema: report of 2 cases. Clin Nephrol. 1989;31(5):259–63.PubMed
23.
Agostoni A, Cicardi M. Hereditary and acquired C1-inhibitor deficiency: biological and clinical characteristics in 235 patients. Medicine. 1992;71(4):206–15.PubMedCrossRef
24.
Farkas H, Csuka D, Gacs J, Czaller I, Zotter Z, Fust G, et al. Lack of increased prevalence of immunoregulatory disorders in hereditary angioedema due to C1-inhibitor deficiency. Clin Immunol. 2011;141(1):58–66.PubMedCrossRef
25.
26.
Brickman CM, Tsokos GC, Balow JE, Lawley TJ, Santaella M, Hammer CH, et al. Immunoregulatory disorders associated with hereditary angioedema. I. Clinical manifestations of autoimmune disease. J Allergy Clin Immunol. 1986;77(5):749–57.PubMedCrossRef
27.
Hayter SM, Cook MC. Updated assessment of the prevalence, spectrum and case definition of autoimmune disease. Autoimmun Rev. 2012;11(10):754–65.PubMedCrossRef
28.
Ricklin D. Manipulating the mediator: modulation of the alternative complement pathway C3 convertase in health, disease and therapy. Immunobiology. 2012;217(11):1057–66.PubMedPubMedCentralCrossRef
29.
Merle NS, Noe R, Halbwachs-Mecarelli L, Fremeaux-Bacchi V, Roumenina LT. Complement system part II: role in immunity. Front Immunol. 2015;6:257.PubMedPubMedCentral
30.
31.
Donaldson VH, Bissler JJ, Welch TR, Burton MF, Davis AE 3rd. Antibody to C1-inhibitor in a patient receiving C1-inhibitor infusions for treatment of hereditary angioneurotic edema with systemic lupus erythematosus reacts with a normal allotype of residue 458 of C1-inhibitor. J Lab Clin Med. 1996;128(4):438–43.PubMedCrossRef
32.
Leru P, Zamfirescu M, Baicus C. Autoimmunity associated with a clear family history of hereditary angioedema. Allergy. 2009;64:254–5.CrossRef
33.
Khan S, Tarzi MD, Dore PC, Sewell WA, Longhurst HJ. Secondary systemic lupus erythematosus: an analysis of 4 cases of uncontrolled hereditary angioedema. Clin Immunol. 2007;123(1):14–7.PubMedCrossRef
34.
Liesmaa I, Paakkanen R, Jarvinen A, Valtonen V, Lokki ML. Clinical features of patients with homozygous complement C4A or C4B deficiency. PLoS ONE. 2018;13(6):e0199305.PubMedPubMedCentralCrossRef
35.
Tsukamoto H, Horiuchi T, Kokuba H, Nagae S, Nishizaka H, Sawabe T, et al. Molecular analysis of a novel hereditary C3 deficiency with systemic lupus erythematosus. Biochem Biophys Res Commun. 2005;330(1):298–304.PubMedCrossRef
36.
Yang Y, Lhotta K, Chung EK, Eder P, Neumair F, Yu CY. Complete complement components C4A and C4B deficiencies in human kidney diseases and systemic lupus erythematosus. J Immunol. 2004;173(4):2803–14.PubMedCrossRef
37.
Sullivan KE, Petri MA, Schmeckpeper BJ, McLean RH, Winkelstein JA. Prevalence of a mutation causing C2 deficiency in systemic lupus erythematosus. J Rheumatol. 1994;21(6):1128–33.PubMed
38.
Holtman JH, Neustadt DH, Klein J, Callen JP. Dapsone is an effective therapy for the skin lesions of subacute cutaneous lupus erythematosus and urticarial vasculitis in a patient with C2 deficiency. J Rheumatol. 1990;17(9):1222–5.PubMed
39.
Hersey P, Lawrence S, Prendergast D, Bindon C, Benson W, Valk P. Association of Sjogren’s syndrome with C4 deficiency, defective reticuloendothelial function and circulating immune complexes. Clin Exp Immunol. 1983;52(3):551–60.PubMedPubMedCentral
40.
Hoppenreijs EP, van Dijken PJ, Kabel PJ, Th Draaisma JM. Hereditary C1q deficiency and secondary Sjogren’s syndrome. Ann Rheum Dis. 2004;63(11):1524–5.PubMedPubMedCentralCrossRef
41.
Rigby WF, Wu YL, Zan M, Zhou B, Rosengren S, Carlson C, et al. Increased frequency of complement C4B deficiency in rheumatoid arthritis. Arthritis Rheum. 2012;64(5):1338–44.PubMedPubMedCentralCrossRef
42.
Schifferli JA, Taylor RP. Physiological and pathological aspects of circulating immune complexes. Kidney Int. 1989;35(4):993–1003.PubMedCrossRef
43.
Garcia-Carrasco M, Pinto CM, Poblano JCS, Morales IE, Cervera R, Anaya JM. Systemic lupus erthematosus. In: Anaya JM, Shoenfeld Y, Rojas-Villarraga A, editors. Autoimmunity: from bench to bedside. Bogota: El Rosario University Press; 2013.
44.
Mincer DL, Jialal I. Hashimoto thyroiditis. In: StatPearls. Treasure Island, FL: StatPearls Publishing LLC; 2018.
45.
46.
Derksen V, Huizinga TWJ, van der Woude D. The role of autoantibodies in the pathophysiology of rheumatoid arthritis. Semin Immunopathol. 2017;39(4):437–46.PubMedPubMedCentralCrossRef
47.
Hansen A, Lipsky PE, Dorner T. Immunopathogenesis of primary Sjogren’s syndrome: implications for disease management and therapy. Curr Opin Rheumatol. 2005;17(5):558–65.PubMedCrossRef
48.
James JA, Harley JB, Scofield RH. Role of viruses in systemic lupus erythematosus and Sjogren syndrome. Curr Opin Rheumatol. 2001;13(5):370–6.PubMedCrossRef
49.
Effraimidis G, Wiersinga WM. Mechanisms in endocrinology: autoimmune thyroid disease: old and new players. Eur J Endocrinol. 2014;170(6):R241–52.PubMedCrossRef
50.
51.
Markovic SN, Inwards DJ, Frigas EA, Phyliky RP. Acquired C1 esterase inhibitor deficiency. Ann Intern Med. 2000;132(2):144–50.PubMedCrossRef
52.
Tekin ZE, Yener GO, Yuksel S. Acquired angioedema in juvenile systemic lupus erythematosus: case-based review. Rheumatol Int. 2018;38(8):1577–84.PubMedCrossRef
53.
Tran JP, McCracken JL, Morsy A, Gonzalez EB. Systemic lupus erythematous presenting as acquired angioedema: a case report and review of the literature. J Autoimmune Syst Dis. 2017;1(1):1000002.
54.
Guilarte M, Luengo O, Nogueiras C, Labrador-Horrillo M, Munoz E, Lopez A, et al. Acquired angioedema associated with hereditary angioedema due to C1 inhibitor deficiency. J Investig Allergol Clin Immunol. 2008;18(2):126–30.PubMed
55.
Longhurst H, Cicardi M, Craig T, Bork K, Grattan C, Baker J, et al. Prevention of Hereditary Angioedema Attacks with a Subcutaneous C1 Inhibitor. N Engl J Med. 2017;376(12):1131–40.PubMedCrossRef
56.
Craig T, Zuraw B, Longhurst H, Cicardi M, Bork K, Grattan C, et al. Long-term outcomes with subcutaneous C1-inhibitor replacement therapy for prevention of hereditary angioedema attacks. J Allergy Clin Immunol Pract. 2019;7(6):1793–802.PubMedCrossRef
57.
Pawaskar D, Tortorici MA, Zuraw B, Craig T, Cicardi M, Longhurst H, et al. Population pharmacokinetics of subcutaneous C1-inhibitor for prevention of attacks in patients with hereditary angioedema. Clin Exp Allergy. 2018;48(10):1325–32.CrossRefPubMed
Metadata
Title
Co-occurrence between C1 esterase inhibitor deficiency and autoimmune disease: a systematic literature review
Authors
Donald Levy
Timothy Craig
Paul K. Keith
Girishanthy Krishnarajah
Rachel Beckerman
Subhransu Prusty
Publication date
01-12-2020

Other articles of this Issue 1/2020

Allergy, Asthma & Clinical Immunology 1/2020 Go to the issue

Research

Exposure to Toxocara spp. and Ascaris lumbricoides infections and risk of allergic rhinitis in children

Case report

A rare case of anaphylaxis to Indian jujube (Ziziphus Mauritiana Lam)

Research

Epidermal growth factor upregulates expression of MUC5AC via TMEM16A, in chronic rhinosinusitis with nasal polyps

Research

A single centre retrospective study of systemic reactions to subcutaneous immunotherapy

Research

Altered vaginal microbiome and relative co-abundance network in pregnant women with penicillin allergy

Letter to the editor

Skin testing with bendamustine: what concentration should be used?