Top

Clinical Rheumatology

Published in:

01-02-2021 | Systemic Lupus Erythematosus | Original Article

Patients with asthma have a higher risk of systemic lupus erythematosus: a systematic review and meta-analysis

Authors: Nipith Charoenngam, Ben Ponvilawan, Wasit Wongtrakul, Patompong Ungprasert

Published in: Clinical Rheumatology | Issue 2/2021

Abstract

Objective

This study aimed to investigate the association between asthma and risk of systemic lupus erythematosus (SLE) using systematic review and meta-analysis technique.

Methods

Potentially eligible studies were identified from Medline and EMBASE databases from inception to March 2020 using search strategy that comprised of terms for “asthma” and “systemic lupus erythematosus.” Qualified cohort study must consist of one cohort of patients with asthma and another cohort of individuals without asthma. Then, the study must report relative risk (RR) with 95% confidence intervals (95% CIs) of incident SLE between the two groups. Qualified case–control studies must consist of cases with SLE and controls without SLE. Then, the study must explore their history of asthma. Odds ratio (OR) with 95% CIs of the association between asthma status and SLE must be reported. Point estimates and standard errors were extracted from each study and were combined using the generic inverse variance method.

Results

A total of 21,486 articles were identified. After two rounds of independent review by three investigators, three cohort studies and seven case–control studies met the eligibility criteria and were included into the meta-analysis. Patients with asthma had a significantly higher risk of SLE compared with individuals without asthma with the pooled odds ratio of 1.37 (95% CI 1.14–1.65; I² 67%). Funnel plot was symmetric and did not suggest the presence of publication bias.

Conclusions

The current study found a significant association between asthma and increased risk of SLE.

Key Points

• Studies have suggested an elevated risk of systemic lupus erythematosus among patients with asthma; however, the results from existing studies are inconsistent.

• This meta-analysis included data from three cohort studies and seven case-–control studies.

• A significant association between asthma and elevated risk of systemic lupus erythematosus was observed, with the pooled odds ratio of 1.37 (95% CI 1.14–1.65; I² 67%).

Available only for authorised users

Maidhof W, Hilas O (2012) Lupus: an overview of the disease and management options. P T 37(4):240–249PubMedPubMedCentral

Rees F, Doherty M, Grainge MJ, Lanyon P, Zhang W (2017) The worldwide incidence and prevalence of systemic lupus erythematosus: a systematic review of epidemiological studies. Rheumatology 56(11):1945–1961. https://doi.org/10.1093/rheumatology/kex260CrossRefPubMed

Weckerle CE, Niewold TB (2011) The unexplained female predominance of systemic lupus erythematosus: clues from genetic and cytokine studies. Clin Rev Allergy Immunol 40(1):42–49. https://doi.org/10.1007/s12016-009-8192-4CrossRefPubMedPubMedCentral

Kamen DL (2014) Environmental influences on systemic lupus erythematosus expression. Rheum Dis Clin North Am 40 (3):401-vii. :https://doi.org/10.1016/j.rdc.2014.05.003

Mims JW (2015) Asthma: definitions and pathophysiology. International forum of allergy & rhinology 5 Suppl 1:S2-6. :https://doi.org/10.1002/alr.21609

Papi A, Brightling C, Pedersen SE, Reddel HK (2018) Asthma. The Lancet 391 (10122):783-800. :https://doi.org/10.1016/S0140-6736(17)33311-1

Anandan C, Nurmatov U, van Schayck OC, Sheikh A (2010) Is the prevalence of asthma declining? Systematic review of epidemiological studies. Allergy 65(2):152–167. https://doi.org/10.1111/j.1398-9995.2009.02244.xCrossRefPubMed

Loftus PA, Wise SK (2016) Epidemiology of asthma. Current opinion in otolaryngology & head and neck surgery 24(3):245–249. https://doi.org/10.1097/moo.0000000000000262CrossRef

Vital signs: asthma prevalence, disease characteristics, and self-management education: United States, 2001--2009 (2011). MMWR Morb Mortal Wkly Rep 60 (17):547–552

10.

Rayner L, McGovern A, Creagh-Brown B, Woodmansey C, de Lusignan S (2019) Type 2 diabetes and asthma: systematic review of the bidirectional relationship. Current diabetes reviews 15(2):118–126. https://doi.org/10.2174/1573399814666180711114859CrossRefPubMed

11.

Kuenzig ME, Bishay K, Leigh R, Kaplan GG, Benchimol EI, Crowdscreen SRRT (2018) Co-occurrence of asthma and the inflammatory bowel diseases: a systematic review and meta-analysis. Clin Transl Gastroenterol 9(9):188. https://doi.org/10.1038/s41424-018-0054-zCrossRefPubMedPubMedCentral

12.

Liu H, Fu Y, Wang K (2017) Asthma and risk of coronary heart disease: a meta-analysis of cohort studies. Annals of allergy, asthma & immunology : official publication of the American College of Allergy, Asthma, & Immunology 118 (6):689-695. :https://doi.org/10.1016/j.anai.2017.03.012

13.

Goldman JA, Klimek GA, Ali R (1976) Allergy in systemic lupus erythematosus. IgE levels and reaginic phenomenon. Arthritis Rheum 19(4):669–676CrossRefPubMed

14.

Sequeira JF, Cesic D, Keser G, Bukelica M, Karanagnostis S, Khamashta MA, Hughes GRV (1993) Allergic disorders in systemic lupus erythematosus. 2 (3):187-191:10.1177/096120339300200311

15.

Morton S, Palmer B, Muir K, Powell RJ (1998) IgE and non-IgE mediated allergic disorders in systemic lupus erythematosus. Annals of the Rheumatic Diseases 57(11):660–663. https://doi.org/10.1136/ard.57.11.660CrossRefPubMedPubMedCentral

16.

Sekigawa I, Yoshiike T, Iida N, Hashimoto H, Ogawa H (2002) Allergic disorders in systemic lupus erythematosus: prevalence and family history. 11 (7):426-429. :https://doi.org/10.1191/0961203302lu221oa

17.

Parks CG, Biagini RE, Cooper GS, Gilkeson GS, Dooley MA (2010) Total serum IgE levels in systemic lupus erythematosus and associations with childhood onset allergies. 19 (14):1614-1622. :https://doi.org/10.1177/0961203310379870

18.

Hsiao YP, Tsai JD, Muo CH, Tsai CH, Sung FC, Liao YT, Chang YJ, Yang JH (2014) Atopic diseases and systemic lupus erythematosus: an epidemiological study of the risks and correlations. International Journal of Environmental Research and Public Health 11(8):8112–8122. https://doi.org/10.3390/ijerph110808112CrossRefPubMedPubMedCentral

19.

Lin CH, Hung PH, Hu HY, Chung CJ, Chen TH, Hung KY (2018) Clinically diagnosed urticaria and risk of systemic lupus erythematosus in children: a nationwide population-based case-control study. Pediatric Allergy and Immunology 29(7):732–739. https://doi.org/10.1111/pai.12962CrossRefPubMed

20.

Hemminki K, Li X, Sundquist J, Sundquist K (2010) Subsequent autoimmune or related disease in asthma patients: clustering of diseases or medical care? Annals of Epidemiology 20(3):217–222. https://doi.org/10.1016/j.annepidem.2009.11.007CrossRefPubMed

21.

Wei CC, Lin CL, Tsai JD, Shen TC, Sung FC (2014) Increased incidence of juvenile onset systemic lupus erythematosus in children with atopic dermatitis. 23 (14):1494-1499. :https://doi.org/10.1177/0961203314543920

22.

Krishna MT, Subramanian A, Adderley NJ, Zemedikun DT, Gkoutos GV, Nirantharakumar K (2019) Allergic diseases and long-term risk of autoimmune disorders: longitudinal cohort study and cluster analysis. European respiratory journal 54 (5). :https://doi.org/10.1183/13993003.00476-2019

23.

Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. European Journal of Epidemiology 25(9):603–605. https://doi.org/10.1007/s10654-010-9491-zCrossRefPubMed

24.

DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188CrossRefPubMed

25.

Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557. https://doi.org/10.1136/bmj.327.7414.557CrossRefPubMedPubMedCentral

26.

Lo CK, Mertz D, Loeb M (2014) Newcastle-Ottawa Scale: comparing reviewers' to authors' assessments. BMC Med Res Methodol 14:45. https://doi.org/10.1186/1471-2288-14-45CrossRefPubMedPubMedCentral

27.

Sekigawa I, Naito T, Hira K, Mitsuishi K, Ogasawara H, Hashimoto H, Ogawa H (2004) Possible mechanisms of gender bias in SLE: a new hypothesis involving a comparison of SLE with atopy. Lupus 13(4):217–222. https://doi.org/10.1191/0961203304lu1012edCrossRefPubMed

28.

Romagnani S (1994) Lymphokine production by human T cells in disease states. Annual Review of Immunology 12(1):227–257. https://doi.org/10.1146/annurev.iy.12.040194.001303CrossRefPubMed

29.

Barnes PJ (2001) Th2 cytokines and asthma: an introduction. Respir Res 2(2):64–65. https://doi.org/10.1186/rr39CrossRefPubMedPubMedCentral

30.

Lourenço EV, La Cava A (2009) Cytokines in systemic lupus erythematosus. Curr Mol Med 9(3):242–254. https://doi.org/10.2174/156652409787847263CrossRefPubMedPubMedCentral

31.

Laurent J, Lagrue G, Sobel A (1986) Increased serum IgE levels in patients with lupus nephritis. American Journal of Nephrology 6(5):413–414. https://doi.org/10.1159/000167202CrossRefPubMed

32.

Charles N, Rivera J (2011) Basophils and autoreactive IgE in the pathogenesis of systemic lupus erythematosus. Curr Allergy Asthma Rep 11 (5):378-387. :https://doi.org/10.1007/s11882-011-0216-5

33.

Dema B, Pellefigues C, Hasni S, Gault N, Jiang C, Ricks TK, Bonelli MM, Scheffel J, Sacré K, Jablonski M, Gobert D, Papo T, Daugas E, Illei G, Charles N, Rivera J (2014) Autoreactive IgE is prevalent in systemic lupus erythematosus and is associated with increased disease activity and nephritis. PLoS One 9(2):e90424. https://doi.org/10.1371/journal.pone.0090424CrossRefPubMedPubMedCentral

34.

Jiménez-Morales S, Velázquez-Cruz R, Ramírez-Bello J, Bonilla-González E, Romero-Hidalgo S, Escamilla-Guerrero G, Cuevas F, Espinosa-Rosales F, Martínez-Aguilar NE, Gómez-Vera J, Baca V, Orozco L (2009) Tumor necrosis factor–α is a common genetic risk factor for asthma, juvenile rheumatoid arthritis, and systemic lupus erythematosus in a Mexican pediatric population. Human Immunology 70(4):251–256. https://doi.org/10.1016/j.humimm.2009.01.027CrossRefPubMed

35.

Mahdi BM, Al-Hadithi ATR, Raouf H, Zalzala HH, Abid LA, Nehad Z (2018) Effect of HLA on development of asthma. Ann Med Surg (Lond) 36:118–121. https://doi.org/10.1016/j.amsu.2018.10.003CrossRef

36.

Ramos PS, Brown EE, Kimberly RP, Langefeld CD (2010) Genetic factors predisposing to systemic lupus erythematosus and lupus nephritis. Semin Nephrol 30(2):164–176. https://doi.org/10.1016/j.semnephrol.2010.01.007CrossRefPubMedPubMedCentral

37.

Rossides M, Nguyen C, Arkema EV, Simard JF (2018) Asthma in children of mothers with systemic lupus erythematosus and the role of preterm birth. Arthritis Care Res (Hoboken) 70(8):1269–1274. https://doi.org/10.1002/acr.23472CrossRef

38.

Stapleton M, Howard-Thompson A, George C, Hoover RM, Self TH (2011) Smoking and asthma. The Journal of the American Board of Family Medicine 24(3):313. https://doi.org/10.3122/jabfm.2011.03.100180CrossRefPubMed

39.

Speyer CB, Costenbader KH (2018) Cigarette smoking and the pathogenesis of systemic lupus erythematosus. Expert Rev Clin Immunol 14(6):481–487. https://doi.org/10.1080/1744666X.2018.1473035CrossRefPubMedPubMedCentral

40.

Costenbader KH, Kim DJ, Peerzada J, Lockman S, Nobles-Knight D, Petri M, Karlson EW (2004) Cigarette smoking and the risk of systemic lupus erythematosus: a meta-analysis. Arthritis & Rheumatism 50(3):849–857. https://doi.org/10.1002/art.20049CrossRef

Title: Patients with asthma have a higher risk of systemic lupus erythematosus: a systematic review and meta-analysis
Authors: Nipith Charoenngam
Ben Ponvilawan
Wasit Wongtrakul
Patompong Ungprasert
Publication date: 01-02-2021
Publisher: Springer International Publishing
Keywords: Systemic Lupus Erythematosus
Bronchial Asthma
Published in: Clinical Rheumatology / Issue 2/2021
Print ISSN: 0770-3198
Electronic ISSN: 1434-9949
DOI: https://doi.org/10.1007/s10067-020-05279-x

ACC 2024 Congress Coverage

Cardiology Video

Highlights from the ACC 2024 Congress

Watch now

Watch official videos from the ACC congress summarizing key highlights from the last year in heart failure, cardiomyopathies, valvular disease, pulmonary vascular disease, and pediatric cardiology.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits

ACC 2024 Pediatric and Congenital Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Pulmonary Vascular Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 Valvular Heart Disease: Year in Review/© 2024 American College of Cardiology, ACC 2024 HF and Cardiomyopathies: Year in Review/© 2024 American College of Cardiology, Woman out walking/© Seventyfour / stock.adobe.com (symbolic image with model), Woman checking smartwatch /© saltdium / stock.adobe.com (symbolic image with model), Cardiac catheterization/© Damian / stock.adobe.com

ACC 2024 Congress

Springer Medicine

Abstract

Objective

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 2/2021

Comparison of the analytical and clinical performances of four anti-cyclic citrullinated peptide antibody assays for diagnosing rheumatoid arthritis

Influence of glutathione S transferase A1 gene polymorphism (-69C > T, rs3957356) on intravenous cyclophosphamide efficacy and side effects: a case-control study in Egyptian patients with lupus nephritis

A multimodal intervention increases influenza vaccine uptake in rheumatoid arthritis

Caution on the masqueraders of Good’s syndrome on thymoma with systemic lupus erythematosus