Semin Respir Crit Care Med
DOI: 10.1055/s-0044-1782653
Review Article

Systemic Lupus Erythematosus-related Lung Disease

Elisabeth Bendstrup
1   Center for Rare Lung Disease, Department of Respiratory Diseases and Allergy, Aarhus University Hospital, Aarhus, Denmark
2   Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
,
Evelyn Lynn
3   Department of Respiratory Medicine, St. Vincent's University Hospital, Dublin, Ireland
4   School of Medicine, University College Dublin, Dublin, Ireland
,
Anne Troldborg
2   Department of Clinical Medicine, Aarhus University, Aarhus, Denmark
5   Department of Rheumatology, Aarhus University Hospital, Aarhus, Denmark
6   Biomedicine, Aarhus University, Aarhus, Denmark
› Author Affiliations

Abstract

Systemic Lupus Erythematosus (SLE) is a multifaceted, multisystem autoimmune disorder with diverse clinical expressions. While prevalence reports vary widely, pulmonary involvement accounts for significant morbidity and mortality in SLE. This comprehensive review explores the spectrum of pulmonary disease in SLE, including upper airway manifestations (e.g., laryngeal affection), lower airway conditions (e.g., bronchitis, bronchiolitis, bronchiectasis), parenchymal diseases (e.g., interstitial lung disease, acute lupus pneumonitis, diffuse alveolar hemorrhage), pleural diseases (e.g., serositis, shrinking lung syndrome), and vascular diseases (e.g., pulmonary arterial hypertension, pulmonary embolism, acute reversible hypoxemia syndrome). We discuss diagnostic modalities, treatment strategies, and prognosis for each pulmonary manifestation. With diagnostics remaining a challenge and with the absence of standardized treatment guidelines, we emphasize the need for evidence-based guidelines to optimize patient care and improve outcomes in this complex disease.



Publication History

Article published online:
28 March 2024

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  • References

  • 1 Kaul A, Gordon C, Crow MK. et al. Systemic lupus erythematosus. Nat Rev Dis Primers 2016; 2: 16039
  • 2 Aringer M, Costenbader K, Daikh D. et al. 2019 EULAR/ACR Classification Criteria for Systemic Lupus Erythematosus. Arthritis Rheumatol 2019; 71 (09) 1400
  • 3 Aguilera-Pickens G, Abud-Mendoza C. Pulmonary manifestations in systemic lupus erythematosus: pleural involvement, acute pneumonitis, chronic interstitial lung disease and diffuse alveolar hemorrhage. Reumatol Clín (Engl Ed) 2018; 14 (05) 294-300
  • 4 Osler W. On the visceral manifestations of the erythema group of skin diseases [Third Paper.] 1904. Am J Med Sci 2009; 338 (05) 396-408
  • 5 Tselios K, Urowitz MB. Cardiovascular and pulmonary manifestations of systemic lupus erythematosus. Curr Rheumatol Rev 2017; 13 (03) 206-218
  • 6 Hannah JR, D'Cruz DP. Pulmonary complications of systemic lupus erythematosus. Semin Respir Crit Care Med 2019; 40 (02) 227-234
  • 7 Kamen DL, Strange C. Pulmonary manifestations of systemic lupus erythematosus. Clin Chest Med 2010; 31 (03) 479-488
  • 8 Narváez J, Borrell H, Sánchez-Alonso F. et al; RELESSER Study Group. Primary respiratory disease in patients with systemic lupus erythematosus: data from the Spanish Rheumatology Society Lupus Registry (RELESSER) cohort. Arthritis Res Ther 2018; 20 (01) 280
  • 9 Gladman DD, Urowitz MB, Caron D. et al. derivation of the sledai. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 1992; 35 (06) 630-640
  • 10 Pines A, Kaplinsky N, Olchovsky D, Rozenman J, Frankl O. Pleuro-pulmonary manifestations of systemic lupus erythematosus: clinical features of its subgroups. Prognostic and therapeutic implications. Chest 1985; 88 (01) 129-135
  • 11 Bertoli AM, Vila LM, Apte M. et al; LUMINA Study Group. Systemic lupus erythematosus in a multiethnic US Cohort LUMINA XLVIII: factors predictive of pulmonary damage. Lupus 2007; 16 (06) 410-417
  • 12 Haye Salinas MJ, Caeiro F, Saurit V. et al; Grupo Latino Americano De Estudio del Lupus (GLADEL). Pleuropulmonary involvement in patients with systemic lupus erythematosus from a Latin American inception cohort (GLADEL). Lupus 2017; 26 (13) 1368-1377
  • 13 Di Bartolomeo S, Alunno A, Carubbi F. Respiratory manifestations in systemic lupus erythematosus. Pharmaceuticals (Basel) 2021; 14 (03) 276
  • 14 Lee JH, Sung IY, Park JH, Roh JL. Recurrent laryngeal neuropathy in a systemic lupus erythematosus (SLE) patient. Am J Phys Med Rehabil 2008; 87 (01) 68-70
  • 15 Teitel AD, MacKenzie CR, Stern R, Paget SA. Laryngeal involvement in systemic lupus erythematosus. Semin Arthritis Rheum 1992; 22 (03) 203-214
  • 16 Karim A, Ahmed S, Siddiqui R, Marder GS, Mattana J. Severe upper airway obstruction from cricoarytenoiditis as the sole presenting manifestation of a systemic lupus erythematosus flare. Chest 2002; 121 (03) 990-993
  • 17 Schwartz IS, Grishman E. Rheumatoid nodules of the vocal cords as the initial manifestation of systemic lupus erythematosus. JAMA 1980; 244 (24) 2751-2752
  • 18 Wohlgelernter D, Loke J, Matthay RA, Siegel NJ. Systemic and discoid lupus erythematosus: analysis of pulmonary function. Yale J Biol Med 1978; 51 (02) 157-164
  • 19 Andonopoulos AP, Constantopoulos SH, Galanopoulou V, Drosos AA, Acritidis NC, Moutsopoulos HM. Pulmonary function of nonsmoking patients with systemic lupus erythematosus. Chest 1988; 94 (02) 312-315
  • 20 Carmier D, Marchand-Adam S, Diot P, Diot E. Respiratory involvement in systemic lupus erythematosus. Rev Mal Respir 2010; 27 (08) e66-e78
  • 21 Kinney WW, Angelillo VA. Bronchiolitis in systemic lupus erythematosus. Chest 1982; 82 (05) 646-649
  • 22 Carmier D, Marchand-Adam S, Diot P, Diot E. [Respiratory involvement in systemic lupus erythematosus]. Rev Mal Respir 2008; 25 (10) 1289-1303
  • 23 Luo Y, Fan X, Jiang C. et al. Systemic lupus erythematosus and angioedema: a cross-sectional study from the national inpatient sample. Arch Rheumatol 2019; 34 (03) 301-307
  • 24 Kumar N, Surendran D, Bammigatti C. Angioedema as the presenting feature of systemic lupus erythematosus. BMJ Case Rep 2018; 2018: bcr2018224222
  • 25 Todic J, Leuchter I. Lupus of the larynx: when bamboo nodes lead to diagnosis…. BMJ Case Rep 2018; 2018: bcr2017221652
  • 26 Bankier AA, Kiener HP, Wiesmayr MN. et al. Discrete lung involvement in systemic lupus erythematosus: CT assessment. Radiology 1995; 196 (03) 835-840
  • 27 Ooi GC, Ngan H, Peh WCG, Mok MY, Ip M. Systemic lupus erythematosus patients with respiratory symptoms: the value of HRCT. Clin Radiol 1997; 52 (10) 775-781
  • 28 Fenlon HM, Doran M, Sant SM, Breatnach E. High-resolution chest CT in systemic lupus erythematosus. AJR Am J Roentgenol 1996; 166 (02) 301-307
  • 29 Silberstein SL, Barland P, Grayzel AI, Koerner SK. Pulmonary dysfunction in systemic lupus erythematosus:prevalence classification and correlation with other organ involvement. J Rheumatol 1980; 7 (02) 187-195
  • 30 Eichacker PQ, Pinsker K, Epstein A, Schiffenbauer J, Grayzel A. Serial pulmonary function testing in patients with systemic lupus erythematosus. Chest 1988; 94 (01) 129-132
  • 31 Rolla G, Brussino L, Bertero MT, Bucca C, Converso M, Caligaris-Cappio F. Respiratory function in systemic lupus erythematosus: relation with activity and severity. Lupus 1996; 5 (01) 38-43
  • 32 Mageau A, Borie R, Crestani B, Timsit JF, Papo T, Sacre K. Epidemiology of interstitial lung disease in systemic lupus erythematosus in France: a nation-wide population-based study over 10 years. Respirology 2022; 27 (08) 630-634
  • 33 Weinrib L, Sharma OP, Quismorio Jr FP. A long-term study of interstitial lung disease in systemic lupus erythematosus. Semin Arthritis Rheum 1990; 20 (01) 48-56
  • 34 Enomoto N, Egashira R, Tabata K. et al. Analysis of systemic lupus erythematosus-related interstitial pneumonia: a retrospective multicentre study. Sci Rep 2019; 9 (01) 7355
  • 35 Sahu D, Saha S, Bhattacherjee S, Datta S, Banik S. Pulmonary involvement in systemic lupus erythematosus patients in a tertiary care hospital. J Assoc Physicians India 2022; 70 (12) 11-12
  • 36 Haupt HM, Moore GW, Hutchins GM. The lung in systemic lupus erythematosus. Analysis of the pathologic changes in 120 patients. Am J Med 1981; 71 (05) 791-798
  • 37 Kondoh Y, Makino S, Ogura T. et al; Joint Committee of Japanese Respiratory Society and Japan College of Rheumatology. 2020 guide for the diagnosis and treatment of interstitial lung disease associated with connective tissue disease. Respir Investig 2021; 59 (06) 709-740
  • 38 Flaherty KR, Wells AU, Cottin V. et al; INBUILD Trial Investigators. Nintedanib in progressive fibrosing interstitial lung diseases. N Engl J Med 2019; 381 (18) 1718-1727
  • 39 Wan SA, Teh CL, Jobli AT. Lupus pneumonitis as the initial presentation of systemic lupus erythematosus: case series from a single institution. Lupus 2016; 25 (13) 1485-1490
  • 40 Matthay RA, Schwarz MI, Petty TL. et al. Pulmonary manifestations of systemic lupus erythematosus: review of twelve cases of acute lupus pneumonitis. Medicine (Baltimore) 1975; 54 (05) 397-409
  • 41 Crestani B. The respiratory system in connective tissue disorders. Allergy 2005; 60 (06) 715-734
  • 42 Chetan G, Mahadevan S, Sulanthung K, Narayanan P. Intravenous immunoglobulin therapy of lupus pneumonitis. Indian J Pediatr 2007; 74 (11) 1032-1033
  • 43 Lim SW, Gillis D, Smith W, Hissaria P, Greville H, Peh CA. Rituximab use in systemic lupus erythematosus pneumonitis and a review of current reports. Intern Med J 2006; 36 (04) 260-262
  • 44 Law AHN, Chuah TY, Lee W. et al. Diffuse alveolar haemorrhage in systemic lupus erythematosus: a multicentre retrospective study in Singapore. Lupus 2023; 32 (08) 952-963
  • 45 Kim D, Choi J, Cho SK. et al. Clinical characteristics and outcomes of diffuse alveolar hemorrhage in patients with systemic lupus erythematosus. Semin Arthritis Rheum 2017; 46 (06) 782-787
  • 46 Andrade C, Mendonça T, Farinha F. et al. Alveolar hemorrhage in systemic lupus erythematosus: a cohort review. Lupus 2016; 25 (01) 75-80
  • 47 Xu T, Zhang G, Lin H. et al. Clinical characteristics and risk factors of diffuse alveolar hemorrhage in systemic lupus erythematosus: a systematic review and meta-analysis based on observational studies. Clin Rev Allergy Immunol 2020; 59 (03) 295-303
  • 48 Kwok SK, Moon SJ, Ju JH. et al. Diffuse alveolar hemorrhage in systemic lupus erythematosus: risk factors and clinical outcome: results from affiliated hospitals of Catholic University of Korea. Lupus 2011; 20 (01) 102-107
  • 49 Martinez-Martinez MU, Sturbaum AK, Alcocer-Varela J. et al. Factors associated with mortality and infections in patients with systemic lupus erythematosus with diffuse alveolar hemorrhage. J Rheumatol 2014; 41 (08) 1656-1661
  • 50 Rojas-Serrano J, Pedroza J, Regalado J. et al. High prevalence of infections in patients with systemic lupus erythematosus and pulmonary haemorrhage. Lupus 2008; 17 (04) 295-299
  • 51 Pego-Reigosa JM, Medeiros DA, Isenberg DA. Respiratory manifestations of systemic lupus erythematosus: old and new concepts. Best Pract Res Clin Rheumatol 2009; 23 (04) 469-480
  • 52 Good Jr JT, King TE, Antony VB, Sahn SA. Lupus pleuritis. Clinical features and pleural fluid characteristics with special reference to pleural fluid antinuclear antibodies. Chest 1983; 84 (06) 714-718
  • 53 Choi BY, Yoon MJ, Shin K, Lee YJ, Song YW. Characteristics of pleural effusions in systemic lupus erythematosus: differential diagnosis of lupus pleuritis. Lupus 2015; 24 (03) 321-326
  • 54 Amarnani R, Yeoh SA, Denneny EK, Wincup C. Lupus and the lungs: the assessment and management of pulmonary manifestations of systemic lupus erythematosus. Front Med (Lausanne) 2021; 7: 610257
  • 55 Wang DY. Diagnosis and management of lupus pleuritis. Curr Opin Pulm Med 2002; 8 (04) 312-316
  • 56 Alamoudi OSB, Attar SM. Pulmonary manifestations in systemic lupus erythematosus: association with disease activity. Respirology 2015; 20 (03) 474-480
  • 57 Sharma S, Smith R, Al-Hameed F. Fibrothorax and severe lung restriction secondary to lupus pleuritis and its successful treatment by pleurectomy. Can Respir J 2002; 9 (05) 335-337
  • 58 Palavutitotai N, Buppajarntham T, Katchamart W. Etiologies and outcomes of pleural effusions in patients with systemic lupus erythematosus. J Clin Rheumatol 2014; 20 (08) 418-421
  • 59 Fanouriakis A, Kostopoulou M, Andersen J. et al. EULAR recommendations for the management of systemic lupus erythematosus: 2023 update. Ann Rheum Dis 2024; 83 (01) 15-29
  • 60 McKnight KM, Adair NE, Agudelo CA. Successful use of tetracycline pleurodesis to treat massive pleural effusion secondary to systemic lupus erythematosus. Arthritis Rheum 1991; 34 (11) 1483-1484
  • 61 Glazer M, Berkman N, Lafair JS, Kramer MR. Successful talc slurry pleurodesis in patients with nonmalignant pleural effusion. Chest 2000; 117 (05) 1404-1409
  • 62 Hoffbrand BI, Beck ER. “Unexplained” dyspnoea and shrinking lungs in systemic lupus erythematosus. BMJ 1965; 1 (5445) 1273-1277
  • 63 Duron L, Cohen-Aubart F, Diot E. et al. Shrinking lung syndrome associated with systemic lupus erythematosus: a multicenter collaborative study of 15 new cases and a review of the 155 cases in the literature focusing on treatment response and long-term outcomes. Autoimmun Rev 2016; 15 (10) 994-1000
  • 64 Toya SP, Tzelepis GE. Association of the shrinking lung syndrome in systemic lupus erythematosus with pleurisy: a systematic review. Semin Arthritis Rheum 2009; 39 (01) 30-37
  • 65 Chick TW, DeHoratius RJ, Skipper BE, Messner RP. Pulmonary dysfunction in systemic lupus erythematosus without pulmonary symptoms. J Rheumatol 1976; 3 (03) 262-268
  • 66 Almajed MR, Obri MS, Mahmood S, Demertzis ZD. Shrinking lung syndrome in a young female: a rare pulmonary manifestation of systemic lupus erythematosus. Cureus 2022; 14 (04) e24320
  • 67 Tavoni A, Vitali C, Cirigliano G, Frigelli S, Stampacchia G, Bombardieri S. Shrinking lung in primary Sjögren's syndrome. Arthritis Rheum 1999; 42 (10) 2249-2250
  • 68 Ahmed S, Herrick A, O'Driscoll BR. Shrinking lung syndrome in patients without systemic lupus erythematosus: comment on the concise communication by Tavoni et al. Arthritis Rheum 2001; 44 (01) 243-245
  • 69 Singh R, Huang W, Menon Y, Espinoza LR. Shrinking lung syndrome in systemic lupus erythematosus and Sjogren's syndrome. J Clin Rheumatol 2002; 8 (06) 340-345
  • 70 Scirè CA, Caporali R, Zanierato M, Mojoli F, Braschi A, Montecucco C. Shrinking lung syndrome in systemic sclerosis. Arthritis Rheum 2003; 48 (10) 2999-3000
  • 71 Calderaro DC, Ferreira GA. Presentation and prognosis of shrinking lung syndrome in systemic lupus erythematosus: report of four cases. Rheumatol Int 2012; 32 (05) 1391-1396
  • 72 Warrington KJ, Moder KG, Brutinel WM. The shrinking lungs syndrome in systemic lupus erythematosus. Mayo Clin Proc 2000; 75 (05) 467-472
  • 73 Hardy K, Herry I, Attali V, Cadranel J, Similowski T. Bilateral phrenic paralysis in a patient with systemic lupus erythematosus. Chest 2001; 119 (04) 1274-1277
  • 74 Pérez-de-Llano LA, Castro-Añón O, López MJ, Escalona E, Teijeira S, Sánchez-Andrade A. Shrinking lung syndrome caused by lupus myopathy. QJM 2011; 104 (03) 259-262
  • 75 Rubin LA, Urowitz MB. Shrinking lung syndrome in SLE–a clinical pathologic study. J Rheumatol 1983; 10 (06) 973-976
  • 76 Laroche CM, Mulvey DA, Hawkins PN. et al. Diaphragm strength in the shrinking lung syndrome of systemic lupus erythematosus. Q J Med 1989; 71 (265) 429-439
  • 77 Hawkins P, Davison AG, Dasgupta B, Moxham J. Diaphragm strength in acute systemic lupus erythematosus in a patient with paradoxical abdominal motion and reduced lung volumes. Thorax 2001; 56 (04) 329-330
  • 78 Omdal R, Roos P, Wildhagen K, Gunnarsson R. Respiratory arrest in systemic lupus erythematosus due to phrenic nerve neuropathy. Lupus 2004; 13 (10) 817-819
  • 79 Wilcox PG, Stein HB, Clarke SD, Paré PD, Pardy RL. Phrenic nerve function in patients with diaphragmatic weakness and systemic lupus erythematosus. Chest 1988; 93 (02) 352-358
  • 80 Roy F, Korathanakhun P, Karamchandani J. et al. Myositis with prominent B-cell aggregates causing shrinking lung syndrome in systemic lupus erythematosus: a case report. BMC Rheumatol 2022; 6 (01) 11
  • 81 Weissman BA, Fatt I. Cancellation of the boundary and edge effects by choice of lens thickness during oxygen permeability measurement of contact lenses. Optom Vis Sci 1989; 66 (05) 264-268
  • 82 Karim MY, Miranda LC, Tench CM. et al. Presentation and prognosis of the shrinking lung syndrome in systemic lupus erythematosus. Semin Arthritis Rheum 2002; 31 (05) 289-298
  • 83 Satış H, Cindil E, Salman RB. et al. Diaphragmatic muscle thickness and diaphragmatic function are reduced in patients with systemic lupus erythematosus compared to those with primary Sjögren's syndrome. Lupus 2020; 29 (07) 715-720
  • 84 Borrell H, Narváez J, Alegre JJ. et al. Shrinking lung syndrome in systemic lupus erythematosus: a case series and review of the literature. Medicine (Baltimore) 2016; 95 (33) e4626
  • 85 Langenskiöld E, Bonetti A, Fitting JW. et al. Shrinking lung syndrome successfully treated with rituximab and cyclophosphamide. Respiration 2012; 84 (02) 144-149
  • 86 Pillai S, Mehta J, Levin T, Muzumdar H, Nandalike K. Shrinking lung syndrome presenting as an initial pulmonary manifestation of SLE. Lupus 2014; 23 (11) 1201-1203
  • 87 Humbert M, Kovacs G, Hoeper MM. et al. 2022 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension. Eur Respir J 2023;61(01):
  • 88 Johnson SR, Gladman DD, Urowitz MB, Ibañez D, Granton JT. Pulmonary hypertension in systemic lupus. Lupus 2004; 13 (07) 506-509
  • 89 Pan TL, Thumboo J, Boey ML. Primary and secondary pulmonary hypertension in systemic lupus erythematosus. Lupus 2000; 9 (05) 338-342
  • 90 Quismorio Jr FP, Sharma O, Koss M. et al. Immunopathologic and clinical studies in pulmonary hypertension associated with systemic lupus erythematosus. Semin Arthritis Rheum 1984; 13 (04) 349-359
  • 91 Shen JY, Chen SL, Wu YX. et al. Pulmonary hypertension in systemic lupus erythematosus. Rheumatol Int 1999; 18 (04) 147-151
  • 92 Simonson JS, Schiller NB, Petri M, Hellmann DB. Pulmonary hypertension in systemic lupus erythematosus. J Rheumatol 1989; 16 (07) 918-925
  • 93 Winslow TM, Ossipov MA, Fazio GP, Simonson JS, Redberg RF, Schiller NB. Five-year follow-up study of the prevalence and progression of pulmonary hypertension in systemic lupus erythematosus. Am Heart J 1995; 129 (03) 510-515
  • 94 Dhala A. Pulmonary arterial hypertension in systemic lupus erythematosus: current status and future direction. Clin Dev Immunol 2012; 2012: 854941
  • 95 Prabu A, Patel K, Yee CS. et al. Prevalence and risk factors for pulmonary arterial hypertension in patients with lupus. Rheumatology (Oxford) 2009; 48 (12) 1506-1511
  • 96 Lv TT, Wang P, Guan SY. et al. Prevalence of pulmonary hypertension in systemic lupus erythematosus: a meta-analysis. Ir J Med Sci 2018; 187 (03) 723-730
  • 97 Li EK, Tam LS. Pulmonary hypertension in systemic lupus erythematosus: clinical association and survival in 18 patients. J Rheumatol 1999; 26 (09) 1923-1929
  • 98 Pope J. An update in pulmonary hypertension in systemic lupus erythematosus - do we need to know about it?. Lupus 2008; 17 (04) 274-277
  • 99 Depascale R, Del Frate G, Gasparotto M. et al. Diagnosis and management of lung involvement in systemic lupus erythematosus and Sjögren's syndrome: a literature review. Ther Adv Musculoskelet Dis 2021; 13: X211040696
  • 100 Tselios K, Gladman DD, Urowitz MB. Systemic lupus erythematosus and pulmonary arterial hypertension: links, risks, and management strategies. Open Access Rheumatol 2016; 9: 1-9
  • 101 Kim KJ, Baek IW, Park YJ, Yoon CH, Kim WU, Cho CS. High levels of uric acid in systemic lupus erythematosus is associated with pulmonary hypertension. Int J Rheum Dis 2015; 18 (05) 524-532
  • 102 Hoeper MM, Bogaard HJ, Condliffe R. et al. Definitions and diagnosis of pulmonary hypertension. J Am Coll Cardiol 2013; 62 (25) D42-D50
  • 103 Badesch DB, Hill NS, Burgess G. et al; SUPER Study Group. Sildenafil for pulmonary arterial hypertension associated with connective tissue disease. J Rheumatol 2007; 34 (12) 2417-2422
  • 104 Mok MY, Tsang PL, Lam YM, Lo Y, Wong WS, Lau CS. Bosentan use in systemic lupus erythematosus patients with pulmonary arterial hypertension. Lupus 2007; 16 (04) 279-285
  • 105 Oudiz RJ, Schilz RJ, Barst RJ. et al; Treprostinil Study Group. Treprostinil, a prostacyclin analogue, in pulmonary arterial hypertension associated with connective tissue disease. Chest 2004; 126 (02) 420-427
  • 106 Robbins IM, Gaine SP, Schilz R, Tapson VF, Rubin LJ, Loyd JE. Epoprostenol for treatment of pulmonary hypertension in patients with systemic lupus erythematosus. Chest 2000; 117 (01) 14-18
  • 107 Rubin LJ, Badesch DB, Barst RJ. et al. Bosentan therapy for pulmonary arterial hypertension. N Engl J Med 2002; 346 (12) 896-903
  • 108 Shirai Y, Yasuoka H, Takeuchi T, Satoh T, Kuwana M. Intravenous epoprostenol treatment of patients with connective tissue disease and pulmonary arterial hypertension at a single center. Mod Rheumatol 2013; 23 (06) 1211-1220
  • 109 Humbert M, Coghlan JG, Ghofrani HA. et al. Riociguat for the treatment of pulmonary arterial hypertension associated with connective tissue disease: results from PATENT-1 and PATENT-2. Ann Rheum Dis 2017; 76 (02) 422-426
  • 110 Kuzuya K, Tsuji S, Matsushita M, Ohshima S, Saeki Y. Systemic sclerosis and systemic lupus erythematosus overlap syndrome with pulmonary arterial hypertension successfully treated with immunosuppressive therapy and riociguat. Cureus 2019; 11 (03) e4327
  • 111 Gonzalez-Lopez L, Cardona-Muñoz EG, Celis A. et al. Therapy with intermittent pulse cyclophosphamide for pulmonary hypertension associated with systemic lupus erythematosus. Lupus 2004; 13 (02) 105-112
  • 112 Kommireddy S, Bhyravavajhala S, Kurimeti K. et al. Pulmonary arterial hypertension in systemic lupus erythematosus may benefit by addition of immunosuppression to vasodilator therapy: an observational study. Rheumatology (Oxford) 2015; 54 (09) 1673-1679
  • 113 Prete M, Fatone MC, Vacca A, Racanelli V, Perosa F. Severe pulmonary hypertension as the initial manifestation of systemic lupus erythematosus: a case report and review of the literature. Clin Exp Rheumatol 2014; 32 (02) 267-274
  • 114 Tanaka E, Harigai M, Tanaka M, Kawaguchi Y, Hara M, Kamatani N. Pulmonary hypertension in systemic lupus erythematosus: evaluation of clinical characteristics and response to immunosuppressive treatment. J Rheumatol 2002; 29 (02) 282-287
  • 115 Yusuf HR, Hooper WC, Grosse SD, Parker CS, Boulet SL, Ortel TL. Risk of venous thromboembolism occurrence among adults with selected autoimmune diseases: a study among a U.S. cohort of commercial insurance enrollees. Thromb Res 2015; 135 (01) 50-57
  • 116 Yusuf HR, Hooper WC, Beckman MG, Zhang QC, Tsai J, Ortel TL. Risk of venous thromboembolism among hospitalizations of adults with selected autoimmune diseases. J Thromb Thrombolysis 2014; 38 (03) 306-313
  • 117 Calvo-Alén J, Toloza SMA, Fernández M. et al; LUMINA Study Group. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA). XXV. Smoking, older age, disease activity, lupus anticoagulant, and glucocorticoid dose as risk factors for the occurrence of venous thrombosis in lupus patients. Arthritis Rheum 2005; 52 (07) 2060-2068
  • 118 Wahl DG, Guillemin F, de Maistre E, Perret C, Lecompte T, Thibaut G. Risk for venous thrombosis related to antiphospholipid antibodies in systemic lupus erythematosus–a meta-analysis. Lupus 1997; 6 (05) 467-473
  • 119 Pengo V, Denas G, Zoppellaro G. et al. Rivaroxaban vs warfarin in high-risk patients with antiphospholipid syndrome. Blood 2018; 132 (13) 1365-1371
  • 120 Abramson SB, Dobro J, Eberle MA. et al. Acute reversible hypoxemia in systemic lupus erythematosus. Ann Intern Med 1991; 114 (11) 941-947
  • 121 Martinez-Taboada VM, Blanco R, Armona J, Fernandez-Sueiro JL, Rodriguez-Valverde V. Acute reversible hypoxemia in systemic lupus erythematosus: a new syndrome or an index of disease activity?. Lupus 1995; 4 (04) 259-262
  • 122 Keane MP, Lynch III JP. Pleuropulmonary manifestations of systemic lupus erythematosus. Thorax 2000; 55 (02) 159-166
  • 123 McCool FD, Tzelepis GE. Dysfunction of the diaphragm. N Engl J Med 2012; 366 (10) 932-942
  • 124 Dubé BP, Dres M. Diaphragm dysfunction: diagnostic approaches and management strategies. J Clin Med 2016; 5 (12) 113
  • 125 Mansel JK, Norman JR. Respiratory complications and management of spinal cord injuries. Chest 1990; 97 (06) 1446-1452
  • 126 Borel CO, Guy J. Ventilatory management in critical neurologic illness. Neurol Clin 1995; 13 (03) 627-644
  • 127 Laroche CM, Green M. The diaphragm in SLE. Chest 1988; 94 (05) 1115
  • 128 Torrente-Segarra V, Salman-Monte TC, Rúa-Figueroa Í. et al; RELESSER Study Group of the Spanish Society of Rheumatology (SER) and the Study Group of Systemic Autoimmune Diseases of the SER (EAS-SER). Associated factors to serious infections in a large cohort of juvenile-onset systemic lupus erythematosus from Lupus Registry (RELESSER). Semin Arthritis Rheum 2020; 50 (04) 657-662
  • 129 Schurder J, Goulenok T, Jouenne R. et al. Pneumococcal infection in patients with systemic lupus erythematosus. Joint Bone Spine 2018; 85 (03) 333-336
  • 130 Peng L, Wang Y, Zhao L, Chen T, Huang A. Severe pneumonia in Chinese patients with systemic lupus erythematosus. Lupus 2020; 29 (07) 735-742
  • 131 Luijten RKMAC, Cuppen BVJ, Bijlsma JWJ, Derksen RHWM. Serious infections in systemic lupus erythematosus with a focus on pneumococcal infections. Lupus 2014; 23 (14) 1512-1516
  • 132 Landewé RBM, Kroon FPB, Alunno A. et al. EULAR recommendations for the management and vaccination of people with rheumatic and musculoskeletal diseases in the context of SARS-CoV-2: the November 2021 update. Ann Rheum Dis 2022; 81 (12) 1628-1639
  • 133 Furer V, Rondaan C, Heijstek MW. et al. 2019 update of EULAR recommendations for vaccination in adult patients with autoimmune inflammatory rheumatic diseases. Ann Rheum Dis 2020; 79 (01) 39-52
  • 134 Spagnolo P, Bonniaud P, Rossi G, Sverzellati N, Cottin V. Drug-induced interstitial lung disease. Eur Respir J 2022; 60 (04) 2102776
  • 135 Petri M, Orbai A-M, Alarcón GS. et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum 2012; 64 (08) 2677-2686
  • 136 Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH. The Committee on Prognosis Studies in SLE. Derivation of the SLEDAI. A disease activity index for lupus patients. Arthritis Rheum 1992; 35 (06) 630-640