Infection in systemic lupus erythematosus-associated diffuse alveolar hemorrhage: a potential key to improve outcomes.


Journal

Clinical rheumatology
ISSN: 1434-9949
Titre abrégé: Clin Rheumatol
Pays: Germany
ID NLM: 8211469

Informations de publication

Date de publication:
Jun 2023
Historique:
received: 29 08 2022
accepted: 17 01 2023
revised: 21 12 2022
medline: 24 5 2023
pubmed: 17 2 2023
entrez: 16 2 2023
Statut: ppublish

Résumé

This study aimed to investigate the clinical characteristics, outcomes, and associated factors of patients with systemic lupus erythematosus-associated diffusive alveolar hemorrhage (SLE-DAH) stratified by infection status in a national representative cohort. This single-center retrospective study included 124 consecutive patients with SLE-DAH in a tertiary care center between 2006 and 2021. The diagnosis of DAH was made based on a comprehensive evaluation of clinical manifestations, laboratory and radiologic findings, and bronchoalveolar lavage. Demographics, clinical features, and survival curves were compared between patients with bacterial, non-bacterial, and non-infection groups. Univariate and multivariate logistic regression analyses were performed to determine the factors independently associated with bacterial infection in SLE-DAH. Fifty-eight patients with SLE-DAH developed bacterial infection after DAH occurrence, thirty-two patients developed fungal and/or viral infection, and thirty-four patients were categorized as non-infection. The bacterial infection group have a worse prognosis (OR 3.059, 95%CI 1.469-6.369, p = 0.002) compared with the other two groups, with a mortality rate of 60.3% within 180 days after DAH occurrence. Factors independently associated with bacterial infections in SLE-DAH included hematuria (OR 4.523, 95%CI 1.068-19.155, p = 0.040), hemoglobin drop in the first 24 h after DAH occurred (OR 1.056, 95%CI 1.001-1.115, p = 0.049), and anti-Smith antibody (OR 0.167, 95%CI 0.052-0.535, p = 0.003). Glucocorticoid pulse therapy and cyclophosphamide were administered in more than 50% of patients regardless of their infectious status. According to clinical experience at our hospital and in previous studies, we recommended a comprehensive management algorithm for SLE-DAH based on infection stratification. Infection, especially bacterial infection, is a severe complication and prognostic factor of SLE-DAH. Comprehensive management strategies, including diagnosis, evaluation, treatment, and monitoring, based on infection stratification may fundamentally improve outcomes of patients with SLE-DAH. Key Points • Bacterial infection is an important, but neglected, prognosis factor of systemic lupus erythematosus (SLE)-associated diffusive alveolar hemorrhage (DAH). • Hematuria, hemoglobin drop, and anti-Smith antibody can independently predict bacterial infections in SLE-DAH. • We put forward a comprehensive management algorithm based on infection stratification for SLE-DAH.

Identifiants

pubmed: 36797549
doi: 10.1007/s10067-023-06517-8
pii: 10.1007/s10067-023-06517-8
doi:

Substances chimiques

Hemoglobins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

1573-1584

Subventions

Organisme : Chinese National Key Technology R&D Program, Ministry of Science and Technology
ID : 2021YFC2501301-5
Organisme : Chinese National Key Technology R&D Program, Ministry of Science and Technology
ID : 2017YFC0907601-3
Organisme : Beijing Municipal Science & Technology Commission
ID : No.Z201100005520022
Organisme : Beijing Municipal Science & Technology Commission
ID : 23
Organisme : Beijing Municipal Science & Technology Commission
ID : 25-27
Organisme : CAMS Innovation Fund for Medical Sciences (CIFMS)
ID : 2021-I2M-1-005

Informations de copyright

© 2023. The Author(s), under exclusive licence to International League of Associations for Rheumatology (ILAR).

Références

Narváez J, Borrell H, Sánchez-Alonso F et al (2018) Primary respiratory disease in patients with systemic lupus erythematosus: data from the Spanish rheumatology society lupus registry (RELESSER) cohort. Arthritis Res Ther 20:280. https://doi.org/10.1186/s13075-018-1776-8
doi: 10.1186/s13075-018-1776-8 pubmed: 30567600 pmcid: 6299951
Kim D, Choi J, Cho S-K et al (2017) Clinical characteristics and outcomes of diffuse alveolar hemorrhage in patients with systemic lupus erythematosus. Semin Arthritis Rheum 46:782–787. https://doi.org/10.1016/j.semarthrit.2016.09.004
doi: 10.1016/j.semarthrit.2016.09.004 pubmed: 27745903
Martínez-Martínez MU, Abud-Mendoza C (2011) Predictors of mortality in diffuse alveolar haemorrhage associated with systemic lupus erythematosus. Lupus 20:568–574. https://doi.org/10.1177/0961203310392430
doi: 10.1177/0961203310392430 pubmed: 21558137
Chang MY, Fang JT, Chen YC et al (2002) Diffuse alveolar hemorrhage in systemic lupus erythematosus: a single center retrospective study in Taiwan. Ren Fail 24:791–802. https://doi.org/10.1081/jdi-120015681
doi: 10.1081/jdi-120015681 pubmed: 12472201
Martínez-Martínez MU, Abud-Mendoza C (2014) Hemorragia alveolar difusa en pacientes con lupus eritematoso sistémico. Manifestaciones clínicas, tratamiento y pronóstico. Reumatol Clín 10:248–253. https://doi.org/10.1016/j.reuma.2014.02.002
doi: 10.1016/j.reuma.2014.02.002 pubmed: 24704107
Zamora MR, Warner ML, Tuder R et al (1997) Diffuse alveolar hemorrhage and systemic lupus erythematosus. Clinical presentation, histology, survival, and outcome. Medicine (Baltimore) 76:192–202. https://doi.org/10.1097/00005792-199705000-00005
doi: 10.1097/00005792-199705000-00005 pubmed: 9193454
Badsha H, Teh CL, Kong KO et al (2004) Pulmonary hemorrhage in systemic lupus erythematosus. Semin Arthritis Rheum 33:414–421. https://doi.org/10.1016/j.semarthrit.2003.09.006
doi: 10.1016/j.semarthrit.2003.09.006 pubmed: 15190526
Moreno-Torres V, Martínez-Urbistondo M, Gutiérrez-Rojas A et al (2022) Impact of severe infections in SLE: an observational study from the Spanish national registry. Lupus Sci Med 9:e000711. https://doi.org/10.1136/lupus-2022-000711
Yurkovich M, Vostretsova K, Chen W et al (2014) Overall and cause-specific mortality in patients with systemic lupus erythematosus: a meta-analysis of observational studies. Arthritis Care Res (Hoboken) 66:608–616. https://doi.org/10.1002/acr.22173
doi: 10.1002/acr.22173 pubmed: 24106157
Yang Y, Jiang H, Wang C et al (2021) Clinical Characteristics and prognoses of patients with systemic lupus erythematosus hospitalized for pulmonary infections. Front Med (Lausanne) 8:732681. https://doi.org/10.3389/fmed.2021.732681
doi: 10.3389/fmed.2021.732681 pubmed: 34660641
Jiang M, Chen R, Zhao L et al (2021) Risk factors for mortality of diffuse alveolar hemorrhage in systemic lupus erythematosus: a systematic review and meta-analysis. Arthritis Res Ther 23:57. https://doi.org/10.1186/s13075-021-02435-9
doi: 10.1186/s13075-021-02435-9 pubmed: 33593433 pmcid: 7885396
Mirouse A, Parrot A, Audigier V et al (2020) Severe diffuse alveolar hemorrhage related to autoimmune disease: a multicenter study. Crit Care 24:231. https://doi.org/10.1186/s13054-020-02936-0
doi: 10.1186/s13054-020-02936-0 pubmed: 32423434 pmcid: 7236262
Sun Y, Zhou C, Zhao J et al (2020) Systemic lupus erythematosus-associated diffuse alveolar hemorrhage: a single-center, matched case-control study in China. Lupus 29:795–803. https://doi.org/10.1177/0961203320920715
doi: 10.1177/0961203320920715 pubmed: 32321345
Bhushan A, Choi D, Maresh G et al (2021) Risk factors and outcomes of immune and non-immune causes of diffuse alveolar hemorrhage: a tertiary-care academic single-center experience. Rheumatol Int. https://doi.org/10.1007/s00296-021-04842-2
doi: 10.1007/s00296-021-04842-2 pubmed: 33782747
Papazian L, Klompas M, Luyt C-E (2020) Ventilator-associated pneumonia in adults: a narrative review. Intensive Care Med 46:888–906. https://doi.org/10.1007/s00134-020-05980-0
doi: 10.1007/s00134-020-05980-0 pubmed: 32157357 pmcid: 7095206
Kwok SK, Moon SJ, Ju JH et al (2011) Diffuse alveolar hemorrhage in systemic lupus erythematosus: risk factors and clinical outcome: results from affiliated hospitals of Catholic University of Korea. Lupus 20:102–107. https://doi.org/10.1177/0961203310381511
doi: 10.1177/0961203310381511 pubmed: 20956464
Martinez-Martinez MU, Sturbaum AK, Alcocer-Varela J et al (2014) Factors associated with mortality and infections in patients with systemic lupus erythematosus with diffuse alveolar hemorrhage. J Rheumatol 41:1656–1661. https://doi.org/10.3899/jrheum.130927
doi: 10.3899/jrheum.130927 pubmed: 24986849
di Pasquale M, Ferrer M, Esperatti M et al (2014) Assessment of severity of ICU-acquired pneumonia and association with etiology. Crit Care Med 42:303–312. https://doi.org/10.1097/CCM.0b013e3182a272a2
doi: 10.1097/CCM.0b013e3182a272a2 pubmed: 23989176
Rello J, Ollendorf DA, Oster G et al (2002) Epidemiology and outcomes of ventilator-associated pneumonia in a large US database. Chest 122:2115–2121. https://doi.org/10.1378/chest.122.6.2115
doi: 10.1378/chest.122.6.2115 pubmed: 12475855
Bailey KL, Kalil AC (2015) Ventilator-associated pneumonia (VAP) with multidrug-resistant (MDR) pathogens: optimal treatment? Curr Infect Dis Rep 17:494. https://doi.org/10.1007/s11908-015-0494-5
doi: 10.1007/s11908-015-0494-5 pubmed: 26092246
Huang Y, Jiao Y, Zhang J et al (2018) Microbial etiology and prognostic factors of ventilator-associated pneumonia: a multicenter retrospective study in Shanghai. Clin Infect Dis 67:S146-s152. https://doi.org/10.1093/cid/ciy686
doi: 10.1093/cid/ciy686 pubmed: 30423049
Luyt CE, Hékimian G, Koulenti D et al (2018) Microbial cause of ICU-acquired pneumonia: hospital-acquired pneumonia versus ventilator-associated pneumonia. Curr Opin Crit Care 24:332–338. https://doi.org/10.1097/mcc.0000000000000526
doi: 10.1097/mcc.0000000000000526 pubmed: 30036192
Danza A, Ruiz-Irastorza G (2013) Infection risk in systemic lupus erythematosus patients: susceptibility factors and preventive strategies. Lupus 22:1286–1294. https://doi.org/10.1177/0961203313493032
doi: 10.1177/0961203313493032 pubmed: 24098001
Shen M, Zeng X, Tian X et al (2010) Diffuse alveolar hemorrhage in systemic lupus erythematosus: a retrospective study in China. Lupus 19:1326–1330. https://doi.org/10.1177/0961203310373106
doi: 10.1177/0961203310373106 pubmed: 20647253
Hughson MD, He Z, Henegar J et al (2001) Alveolar hemorrhage and renal microangiopathy in systemic lupus erythematosus. Arch Pathol Lab Med 125:475–483. https://doi.org/10.5858/2001-125-0475-aharmi
doi: 10.5858/2001-125-0475-aharmi pubmed: 11260619
Merola JF, Prystowsky SD, Iversen C et al (2013) Association of discoid lupus erythematosus with other clinical manifestations among patients with systemic lupus erythematosus. J Am Acad Dermatol 69:19–24. https://doi.org/10.1016/j.jaad.2013.02.010
doi: 10.1016/j.jaad.2013.02.010 pubmed: 23541758 pmcid: 3686921
Li PH, Wong WH, Lee TL et al (2013) Relationship between autoantibody clustering and clinical subsets in SLE: cluster and association analyses in Hong Kong Chinese. Rheumatology (Oxford) 52:337–345. https://doi.org/10.1093/rheumatology/kes261
doi: 10.1093/rheumatology/kes261 pubmed: 23038697
Zhao K, Xie H, Li L et al (2021) Increased risk of severe infections and mortality in patients with newly diagnosed systemic lupus erythematosus: a population-based study. Rheumatology (Oxford) 60:5300–5309. https://doi.org/10.1093/rheumatology/keab219
doi: 10.1093/rheumatology/keab219 pubmed: 33751035
Alexandre AT, Vale A, Gomes T (2019) Diffuse alveolar hemorrhage: how relevant is etiology? Sarcoidosis Vasc Diffuse Lung Dis 36:47–52. https://doi.org/10.36141/svdld.v36i1.7160
doi: 10.36141/svdld.v36i1.7160 pubmed: 32476936 pmcid: 7247111
Lichtenberger JP, Digumarthy SR, Abbott GF et al (2014) Diffuse pulmonary hemorrhage: clues to the diagnosis. Curr Probl Diagn Radiol 43:128–139. https://doi.org/10.1067/j.cpradiol.2014.01.002
doi: 10.1067/j.cpradiol.2014.01.002 pubmed: 24791616
Andrade C, Mendonça T, Farinha F et al (2016) Alveolar hemorrhage in systemic lupus erythematosus: a cohort review. Lupus 25:75–80. https://doi.org/10.1177/0961203315605365
doi: 10.1177/0961203315605365 pubmed: 26385219
Martínez-Martínez MU, Oostdam DAH, Abud-Mendoza C (2017) Diffuse alveolar hemorrhage in autoimmune diseases. Curr Rheumatol Rep 19:27. https://doi.org/10.1007/s11926-017-0651-y
doi: 10.1007/s11926-017-0651-y pubmed: 28397125
Barile LA, Jara LJ, Medina-Rodriguez F et al (1997) Pulmonary hemorrhage in systemic lupus erythematosus. Lupus 6:445–448. https://doi.org/10.1177/096120339700600506
doi: 10.1177/096120339700600506 pubmed: 9229363
Ednalino C, Yip J, Carsons SE (2015) Systematic review of diffuse alveolar hemorrhage in systemic lupus erythematosus: focus on outcome and therapy. J Clin Rheumatol 21:305–310. https://doi.org/10.1097/rhu.0000000000000291
doi: 10.1097/rhu.0000000000000291 pubmed: 26308350
Rathi NK, Tanner AR, Dinh A et al (2015) Low-, medium- and high-dose steroids with or without aminocaproic acid in adult hematopoietic SCT patients with diffuse alveolar hemorrhage. Bone Marrow Transplant 50:420–426. https://doi.org/10.1038/bmt.2014.287
doi: 10.1038/bmt.2014.287 pubmed: 25531284
Torres A, Niederman MS, Chastre J et al (2017) International ERS/ESICM/ESCMID/ALAT guidelines for the management of hospital-acquired pneumonia and ventilator-associated pneumonia: Guidelines for the management of hospital-acquired pneumonia (HAP)/ventilator-associated pneumonia (VAP) of the European Respiratory Society (ERS), European Society of Intensive Care Medicine (ESICM), European Society of Clinical Microbiology and Infectious Diseases (ESCMID) and Asociación Latinoamericana del Tórax (ALAT). Eur Respir J 50:1700582. https://doi.org/10.1183/13993003.00582-2017
Kazzaz NM, Coit P, Lewis EE et al (2015) Systemic lupus erythematosus complicated by diffuse alveolar haemorrhage: risk factors, therapy and survival. Lupus Science & Medicine 2:e000117. https://doi.org/10.1136/lupus-2015-000117
doi: 10.1136/lupus-2015-000117
Blay G, Rodrigues JC, Ferreira JCO et al (2018) Diffuse alveolar hemorrhage in childhood-onset systemic lupus erythematosus: a severe disease flare with serious outcome. Adv Rheumatol 58:39. https://doi.org/10.1186/s42358-018-0038-4
doi: 10.1186/s42358-018-0038-4 pubmed: 30657099
Rajagopala S, Sagar BK, Thabah MM et al (2015) Pulmonary-renal syndromes: experience from an Indian intensive care unit. Indian J Crit Care Med 19:316–325. https://doi.org/10.4103/0972-5229.158261
doi: 10.4103/0972-5229.158261 pubmed: 26195857 pmcid: 4478672

Auteurs

Mucong Li (M)

Department of Rheumatology and Clinical Immunology, Chinese Academy of Medical Sciences & Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases (NCRC-DID), Ministry of Science & Technology, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital (PUMCH), Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing, 100730, China.

Wei Bai (W)

Department of Rheumatology and Clinical Immunology, Chinese Academy of Medical Sciences & Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases (NCRC-DID), Ministry of Science & Technology, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital (PUMCH), Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing, 100730, China.

Yanhong Wang (Y)

Department of Epidemiology and Biostatistics, Institute of Basic Medical Sciences Chinese Academy of Medical Sciences, School of Basic Medicine Peking, Union Medical College, Beijing, 100730, China.

Lan Song (L)

Department of Radiology, Peking Union Medical College Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College, Beijing, 100730, China.

Shangzhu Zhang (S)

Department of Rheumatology and Clinical Immunology, Chinese Academy of Medical Sciences & Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases (NCRC-DID), Ministry of Science & Technology, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital (PUMCH), Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing, 100730, China.

Jiuliang Zhao (J)

Department of Rheumatology and Clinical Immunology, Chinese Academy of Medical Sciences & Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases (NCRC-DID), Ministry of Science & Technology, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital (PUMCH), Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing, 100730, China.

Chanyuan Wu (C)

Department of Rheumatology and Clinical Immunology, Chinese Academy of Medical Sciences & Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases (NCRC-DID), Ministry of Science & Technology, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital (PUMCH), Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing, 100730, China. wucy@pumch.cn.

Mengtao Li (M)

Department of Rheumatology and Clinical Immunology, Chinese Academy of Medical Sciences & Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases (NCRC-DID), Ministry of Science & Technology, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital (PUMCH), Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing, 100730, China.

Xinping Tian (X)

Department of Rheumatology and Clinical Immunology, Chinese Academy of Medical Sciences & Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases (NCRC-DID), Ministry of Science & Technology, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital (PUMCH), Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing, 100730, China.

Xiaofeng Zeng (X)

Department of Rheumatology and Clinical Immunology, Chinese Academy of Medical Sciences & Peking Union Medical College, National Clinical Research Center for Dermatologic and Immunologic Diseases (NCRC-DID), Ministry of Science & Technology, State Key Laboratory of Complex Severe and Rare Diseases, Peking Union Medical College Hospital (PUMCH), Key Laboratory of Rheumatology and Clinical Immunology, Ministry of Education, Beijing, 100730, China.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH