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Risk factors and biomarkers for ınterstitial lung disease and pulmonary arterial hypertension in systemic sclerosis: experience of two tertiary centers in Türkiye

Year 2024, , 722 - 731, 09.10.2024
https://doi.org/10.31362/patd.1452076

Abstract

Purpose: To define the clinical and laboratory characteristics of patients with systemic sclerosis (SSc), and to investigate the risk factors affecting the prevalence of interstitial lung disease (ILD) and pulmonary arterial hypertension (PAH), which are important causes of morbidity and mortality.
Patients and methods: 88 patients with SSc were compared according to the presence of ILD and PAH. ILD was confirmed by chest high-resolution computed tomography, and PAH was suspected and considered probable PAH when right ventricular systolic pressure was >40 mmHg according to echocardiography during rest.
Results: Of the 88 patients, 44.3% had diffuse-type and 55.7% had limited-type SSc. Diffuse type, percentages of positive anti-scleroderma-70 (anti-Scl70) antibody and anti-centromere antibody, white blood cell (WBC), platelet, erythrocyte sedimentation rate (ESR), smoking, and presence of the sclerodactyly and telangiectasia differed significantly in SSc with ILD group. The positive titer of anti-Scl70 antibody (odds ratio (OR)=6.124, p=0.004), platelet count (OR=0.138, p=0.002), ESR (OR=1.042, p=0.035) and presence of telangiectasia (OR=10.571, p=0.001) were associated with ILD in patients with SSc. Also, while diffuse-type (OR=0.223, p=0.010), the presence of sclerodactyly (OR=11.112, p=0.028) and telangiectasia (OR=3.861, p=0.020) were risk factors for the development of ILD in nonspecific interstitial pneumonia pattern, anti-Scl-70 antibody positivity (OR=12.921, p=0.019) and high ESR (OR=1.034, p=0.030) were found to be risk factors for the development of usual interstitial pneumonia pattern. When evaluated in terms of PAH, the only risk factor was found to be advanced age (OR=1.073, 95% CI:1.012-1.139, p=0.019).
Conclusion: Positive titer of the anti-Scl70 antibody, diffuse type, presence of telangiectasia, and high ESR
were independently associated with ILD in SSc patients.

Ethical Statement

Permission was obtained from Ondokuz Mayis University Non-Interventional Clinical Research Ethics Committee for the study (Approval number: 2020/742).

References

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  • 2. Cottin V, Brown KK. Interstitial lung disease associated with systemic sclerosis (SSc-ILD). Respir Res 2019;20:13. https://doi.org/10.1186/s12931-019-0980-7
  • 3. Adigun R, Goyal A, Hariz A. Systemic Sclerosis. [Updated 2022 May 8]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan. Available from: https://www.ncbi.nlm.nih.gov/books/NBK430875/. Accessed March 14, 2024
  • 4. Kowal Bielecka O, Fransen J, Avouac J, et al. EUSTAR Coauthors. Update of EULAR recommendations for the treatment of systemic sclerosis. Ann Rheum Dis 2017;76:1327-1339. https://doi.org/10.1136/annrheumdis-2016-209909
  • 5. Elhai M, Meune C, Boubaya M, et al. EUSTAR group. Mapping and predicting mortality from systemic sclerosis. Ann Rheum Dis 2017;76:1897-1905. https://doi.org/10.1136/annrheumdis-2017-211448
  • 6. Denton CP, Khanna D. Systemic sclerosis. Lancet 2017;390:1685-1699. https://doi.org/10.1016/S0140-6736(17)30933-9
  • 7. Sobanski V, Launay D, Hachulla E, Humbert M. Current Approaches to the treatment of Systemic-Sclerosis-Associated Pulmonary Arterial Hypertension (SSc-PAH). Curr Rheumatol Rep 2016;18:10. https://doi.org/10.1007/s11926-015-0560-x
  • 8. Simonneau G, Montani D, Celermajer DS, et al. Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur Respir J 2019;53:1801913. https://doi.org/10.1183/13993003.01913-2018
  • 9. Vachiéry JL, Brimioulle S, Crasset V, Naeije R. False-positive diagnosis of pulmonary hypertension by Doppler echocardiography. Eur Respir J 1998;12:1476-1478. https://doi.org/10.1183/09031936.98.12061476
  • 10. Ferrara, F, Zhou X, Gargani L, et al. Echocardiography in pulmonary arterial hypertension. Curr Cardiol Rep 2019;21:22. https://doi.org/10.1007/s11886-019-1109-9
  • 11. Meune C, Avouac J, Wahbi K, et al. Cardiac involvement in systemic sclerosis assessed by tissue-doppler echocardiography during routine care: a controlled study of 100 consecutive patients. Arthritis Rheum 2008;58:1803-1809. https://doi.org/10.1002/art.23463
  • 12. Yang X, Mardekian J, Sanders KN, Mychaskiw MA, Thomas J 3rd. Prevalence of pulmonary arterial hypertension in patients with connective tissue diseases: a systematic review of the literature. Clin Rheumatol 2013;32:1519-1531. https://doi.org/10.1007/s10067-013-2307-2
  • 13. Hachulla E, Gressin V, Guillevin L, et al. Early detection of pulmonary arterial hypertension in systemic sclerosis: a French nationwide prospective multicenter study. Arthritis Rheum 2005;52:3792-3800. https://doi.org/10.1002/art.21433
  • 14. Hinchcliff M, Fischer A, Schiopu E, Steen VD, PHAROS Investigators. Pulmonary Hypertension Assessment and Recognition of Outcomes in Scleroderma (PHAROS): baseline characteristics and description of study population. J Rheumatol 2011;38:2172-2179. https://doi.org/10.3899/jrheum.101243
  • 15. Coghlan JG, Denton CP, Grünig E, et al. DETECT study group. Evidence-based detection of pulmonary arterial hypertension in systemic sclerosis: the DETECT study. Ann Rheum Dis 2014;73:1340-1349. https://doi.org/10.1136/annrheumdis-2013-203301
  • 16. Kalchiem Dekel O, Galvin JR, Burke AP, Atamas SP, Todd NW. Interstitial lung disease and pulmonary fibrosis: a practical approach for general medicine physicians with focus on the medical history. J Clin Med 2018;7:476. https://doi.org/10.3390/jcm7120476
  • 17. Jaeger VK, Wirz EG, Allanore Y, et al. EUSTAR co-authors. Incidences and risk factors of organ manifestations in the early course of systemic sclerosis: a longitudinal EUSTAR Study. PLoS One 2016;11:e0163894. https://doi.org/10.1371/journal.pone.0163894
  • 18. Steen V, Domsic RT, Lucas M, Fertig N, Medsger TA Jr. A clinical and serologic comparison of African American and Caucasian patients with systemic sclerosis. Arthritis Rheum 2012;64:2986-2994. https://doi.org/10.1002/art.34482
  • 19. Varga J. Systemic sclerosis: an update. Bull NYU Hosp Jt Dis 2008;66:198-202.
  • 20. Bussone G, Mouthon L. Interstitial lung disease in systemic sclerosis. Autoimmun Rev 2011;10:248-255. https://doi.org/10.1016/j.autrev.2010.09.012
  • 21. Masi AT, Subcommittee for scleroderma criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum 1980;23:581-590. https://doi.org/10.1002/art.1780230510
  • 22. Giacomelli R, Liakouli V, Berardicurti O, et al. Interstitial lung disease in systemic sclerosis: current and future treatment. Rheumatol Int 2017;37:853-863. https://doi.org/10.1007/s00296-016-3636-7
  • 23. Meier FM, Frommer KW, Dinser R, et al. EUSTAR Co-authors. Update on the profile of the EUSTAR cohort: an analysis of the EULAR Scleroderma Trials and Research group database. Ann Rheum Dis 2012;71:1355-1360. https://doi.org/10.1136/annrheumdis-2011-200742
  • 24. Walker UA, Tyndall A, Czirják L, et al. Clinical risk assessment of organ manifestations in systemic sclerosis: a report from the EULAR Scleroderma Trials And Research group database. Ann Rheum Dis 2007;66:754-763. https://doi.org/10.1136/ard.2006.062901
  • 25. McNearney TA, Reveille JD, Fischbach M, et al. Pulmonary involvement in systemic sclerosis: associations with genetic, serologic, sociodemographic, and behavioral factors. Arthritis Rheum 2007;57:318-326. https://doi.org/10.1002/art.22532
  • 26. Markusse IM, Meijs J, de Boer B, et al. Predicting cardiopulmonary involvement in patients with systemic sclerosis: complementary value of nailfold videocapillaroscopy patterns and disease-specific autoantibodies. Rheumatology (Oxford) 2017;56:1081-1088. https://doi.org/10.1093/rheumatology/kew402
  • 27. Jung E, Suh CH, Kim HA, Jung JY. Clinical characteristics of systemic sclerosis with ınterstitial lung disease. Arch Rheumatol 2018;33:322-327. https://doi.org/10.5606/ArchRheumatol.2018.6630
  • 28. Ashmore P, Tikly M, Wong M, Ickinger C. Interstitial lung disease in South Africans with systemic sclerosis. Rheumatol Int 2018;38:657-662. https://doi.org/10.1007/s00296-017-3893-0
  • 29. Wangkaew S, Euathrongchit J, Wattanawittawas P, Kasitanon N, Louthrenoo W. Incidence and predictors of interstitial lung disease (ILD) in Thai patients with early systemic sclerosis: inception cohort study. Mod Rheumatol 2016;26:588-593. https://doi.org/10.3109/14397595.2015.1115455
  • 30. Ho KT, Reveille JD. The clinical relevance of autoantibodies in scleroderma. Arthritis Res Ther 2003;5:80-93. https://doi.org/10.1186/ar628
  • 31. Kennedy B, Branagan P, Moloney F, et al. Biomarkers to identify ILD and predict lung function decline in scleroderma lung disease or idiopathic pulmonary fibrosis. Sarcoidosis Vasc Diffuse Lung Dis 2015;32:228-236.
  • 32. Liaskos C, Marou E, Simopoulou T, et al. Disease-related autoantibody profile in patients with systemic sclerosis. Autoimmunity 2017;50:414-421. https://doi.org/10.1080/08916934.2017.1357699
  • 33. Liu X, Mayes MD, Pedroza C, et al. Does C-reactive protein predict the long-term progression of interstitial lung disease and survival in patients with early systemic sclerosis? Arthritis Care Res (Hoboken) 2013;65:1375-1380. https://doi.org/10.1002/acr.21968
  • 34. Mulkoju R, Saka VK, Rajaram M, et al. Pulmonary manifestations in systemic sclerosis: hospital-based descriptive study. Cureus 2020;12:e8649. https://doi.org/10.7759/cureus.8649
  • 35. Avouac J, Airò P, Meune C, et al. Prevalence of pulmonary hypertension in systemic sclerosis in European Caucasians and metaanalysis of 5 studies. J Rheumatol 2010;37:2290-2998. https://doi.org/10.3899/jrheum.100245
  • 36. Erken Pamukcu H, Tunca Ç, Özişler C, et al. Pulmonary hypertension screening in patients with systemic sclerosis, in a tertiary center, in Turkey; a cross-sectional original study. TJCL 2020;11:146-155. https://doi.org/10.18663/tjcl.630633
  • 37. McGoon MD, Benza RL, Escribano Subias P, et al. Pulmonary arterial hypertension: epidemiology and registries. J Am Coll Cardiol 2013;62:51-59. https://doi.org/10.1016/j.jacc.2013.10.023
  • 38. Hachulla E, Launay D. Diagnosis and classification of systemic sclerosis. Clin Rev Allergy Immunol 2011;40:78-83. https://doi.org/10.1007/s12016-010-8198-y
  • 39. Hachulla E, de Groote P, Gressin V, et al. Itinér AIR-Sclérodermie Study Group. The three-year incidence of pulmonary arterial hypertension associated with systemic sclerosis in a multicenter nationwide longitudinal study in France. Arthritis Rheum 2009;60:1831-1839. https://doi.org/10.1002/art.24525
  • 40. Jiang Y, Turk MA, Pope JE. Factors associated with pulmonary arterial hypertension (PAH) in systemic sclerosis (SSc). Autoimmun Rev 2020;19:102602. https://doi.org/10.1016/j.autrev.2020.102602
  • 41. Morrisroe K, Huq M, Stevens W, Rabusa C, Proudman SM, Nikpour M; Australian Scleroderma Interest Group (ASIG). Risk factors for development of pulmonary arterial hypertension in Australian systemic sclerosis patients: results from a large multicenter cohort study. BMC Pulm Med 2016;16:134. https://doi.org/10.1186/s12890-016-0296-z

Sistemik sklerozda interstisyel akciğer hastalığı ve pulmoner arteriyel hipertansiyon için risk faktörleri ve biyobelirteçler: Türkiye'de iki tersiyer merkezin deneyimi

Year 2024, , 722 - 731, 09.10.2024
https://doi.org/10.31362/patd.1452076

Abstract

Amaç: Sistemik skleroz (SSk) hastalarının klinik ve laboratuvar özelliklerini tanımlamak, önemli morbidite ve mortalite nedenleri olan interstisyel akciğer hastalığı (İAH) ve pulmoner arteriyel hipertansiyon (PAH) prevalansını etkileyen risk faktörlerini araştırmak.
Hastalar ve yöntemler: Sistemik skleroz tanısı olan 88 hasta İAH ve PAH varlığına göre karşılaştırıldı. Akciğerin yüksek rezolüsyonlu bilgisayarlı tomografisi ile İAH doğrulandı ve istirahatte uygulanan ekokardiyografiye göre sağ ventriküler sistolik basınç >40 mmHg olduğunda olası PAH olarak değerlendirildi ve kaydedildi.
Bulgular: 88 hastanın %44,3'ünde yaygın tipte ve %55,7'sinde sınırlı tipte SSk vardı. Diffüz tip, pozitif antiskleroderma-70 (anti-Scl70) antikoru ve anti-sentromer antikor yüzdeleri, beyaz kan hücresi, trombosit sayısı, eritrosit sedimantasyon hızı (ESH), sigara içme ve sklerodaktili ve telanjiektazi varlığı İAH olan grupta anlamlı farklı saptandı. Anti-Scl70 antikorunun pozitif titresi (odds oranı (OR)=6,124, p=0,004), trombosit sayısı (OR=0,138, p=0,002), ESH (OR=1,042, p=0,035) ve talenjiektazi varlığı (OR=10,571, p=0,001), SSk'li hastalarda İAH ile ilişkili bulundu. Ayrıca diffüz tip (OR=0,223, p=0,010), sklerodaktili (OR=11,112, p=0,028) ve talenjiektazi (OR=3,861, p=0,020) varlığı nonspesifik interstisyel pnömoni paterninde İAH gelişimi için risk faktörleri iken, anti Scl-70 antikor pozitifliği (OR=12,921, p=0,019) ve yüksek ESH'nın (OR=1,034, p=0,030) usual interstisyel pnömoni paterni gelişimi için risk faktörleri olduğu saptandı. PAH açısından değerlendirildiğinde ise tek risk
faktörünün ileri yaş olduğu görüldü (OR=1,073, %95 GA:1,012-1,139, p=0,019).
Sonuç: Anti Scl-70 antikorunun pozitif titresi, yaygın tip, talenjiektazi varlığı ve yüksek ESH, SSk hastalarında İAH'nın varlığı ile bağımsız olarak ilişkilendirildi.

References

  • 1. Barsotti S, Orlandi M, Codullo V, et al. One year in review 2019: systemic sclerosis. Clin Exp Rheumatol 2019;119:3-14.
  • 2. Cottin V, Brown KK. Interstitial lung disease associated with systemic sclerosis (SSc-ILD). Respir Res 2019;20:13. https://doi.org/10.1186/s12931-019-0980-7
  • 3. Adigun R, Goyal A, Hariz A. Systemic Sclerosis. [Updated 2022 May 8]. In: StatPearls [Internet]. Treasure Island (FL): StatPearls Publishing; 2024 Jan. Available from: https://www.ncbi.nlm.nih.gov/books/NBK430875/. Accessed March 14, 2024
  • 4. Kowal Bielecka O, Fransen J, Avouac J, et al. EUSTAR Coauthors. Update of EULAR recommendations for the treatment of systemic sclerosis. Ann Rheum Dis 2017;76:1327-1339. https://doi.org/10.1136/annrheumdis-2016-209909
  • 5. Elhai M, Meune C, Boubaya M, et al. EUSTAR group. Mapping and predicting mortality from systemic sclerosis. Ann Rheum Dis 2017;76:1897-1905. https://doi.org/10.1136/annrheumdis-2017-211448
  • 6. Denton CP, Khanna D. Systemic sclerosis. Lancet 2017;390:1685-1699. https://doi.org/10.1016/S0140-6736(17)30933-9
  • 7. Sobanski V, Launay D, Hachulla E, Humbert M. Current Approaches to the treatment of Systemic-Sclerosis-Associated Pulmonary Arterial Hypertension (SSc-PAH). Curr Rheumatol Rep 2016;18:10. https://doi.org/10.1007/s11926-015-0560-x
  • 8. Simonneau G, Montani D, Celermajer DS, et al. Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur Respir J 2019;53:1801913. https://doi.org/10.1183/13993003.01913-2018
  • 9. Vachiéry JL, Brimioulle S, Crasset V, Naeije R. False-positive diagnosis of pulmonary hypertension by Doppler echocardiography. Eur Respir J 1998;12:1476-1478. https://doi.org/10.1183/09031936.98.12061476
  • 10. Ferrara, F, Zhou X, Gargani L, et al. Echocardiography in pulmonary arterial hypertension. Curr Cardiol Rep 2019;21:22. https://doi.org/10.1007/s11886-019-1109-9
  • 11. Meune C, Avouac J, Wahbi K, et al. Cardiac involvement in systemic sclerosis assessed by tissue-doppler echocardiography during routine care: a controlled study of 100 consecutive patients. Arthritis Rheum 2008;58:1803-1809. https://doi.org/10.1002/art.23463
  • 12. Yang X, Mardekian J, Sanders KN, Mychaskiw MA, Thomas J 3rd. Prevalence of pulmonary arterial hypertension in patients with connective tissue diseases: a systematic review of the literature. Clin Rheumatol 2013;32:1519-1531. https://doi.org/10.1007/s10067-013-2307-2
  • 13. Hachulla E, Gressin V, Guillevin L, et al. Early detection of pulmonary arterial hypertension in systemic sclerosis: a French nationwide prospective multicenter study. Arthritis Rheum 2005;52:3792-3800. https://doi.org/10.1002/art.21433
  • 14. Hinchcliff M, Fischer A, Schiopu E, Steen VD, PHAROS Investigators. Pulmonary Hypertension Assessment and Recognition of Outcomes in Scleroderma (PHAROS): baseline characteristics and description of study population. J Rheumatol 2011;38:2172-2179. https://doi.org/10.3899/jrheum.101243
  • 15. Coghlan JG, Denton CP, Grünig E, et al. DETECT study group. Evidence-based detection of pulmonary arterial hypertension in systemic sclerosis: the DETECT study. Ann Rheum Dis 2014;73:1340-1349. https://doi.org/10.1136/annrheumdis-2013-203301
  • 16. Kalchiem Dekel O, Galvin JR, Burke AP, Atamas SP, Todd NW. Interstitial lung disease and pulmonary fibrosis: a practical approach for general medicine physicians with focus on the medical history. J Clin Med 2018;7:476. https://doi.org/10.3390/jcm7120476
  • 17. Jaeger VK, Wirz EG, Allanore Y, et al. EUSTAR co-authors. Incidences and risk factors of organ manifestations in the early course of systemic sclerosis: a longitudinal EUSTAR Study. PLoS One 2016;11:e0163894. https://doi.org/10.1371/journal.pone.0163894
  • 18. Steen V, Domsic RT, Lucas M, Fertig N, Medsger TA Jr. A clinical and serologic comparison of African American and Caucasian patients with systemic sclerosis. Arthritis Rheum 2012;64:2986-2994. https://doi.org/10.1002/art.34482
  • 19. Varga J. Systemic sclerosis: an update. Bull NYU Hosp Jt Dis 2008;66:198-202.
  • 20. Bussone G, Mouthon L. Interstitial lung disease in systemic sclerosis. Autoimmun Rev 2011;10:248-255. https://doi.org/10.1016/j.autrev.2010.09.012
  • 21. Masi AT, Subcommittee for scleroderma criteria of the American Rheumatism Association Diagnostic and Therapeutic Criteria Committee. Preliminary criteria for the classification of systemic sclerosis (scleroderma). Arthritis Rheum 1980;23:581-590. https://doi.org/10.1002/art.1780230510
  • 22. Giacomelli R, Liakouli V, Berardicurti O, et al. Interstitial lung disease in systemic sclerosis: current and future treatment. Rheumatol Int 2017;37:853-863. https://doi.org/10.1007/s00296-016-3636-7
  • 23. Meier FM, Frommer KW, Dinser R, et al. EUSTAR Co-authors. Update on the profile of the EUSTAR cohort: an analysis of the EULAR Scleroderma Trials and Research group database. Ann Rheum Dis 2012;71:1355-1360. https://doi.org/10.1136/annrheumdis-2011-200742
  • 24. Walker UA, Tyndall A, Czirják L, et al. Clinical risk assessment of organ manifestations in systemic sclerosis: a report from the EULAR Scleroderma Trials And Research group database. Ann Rheum Dis 2007;66:754-763. https://doi.org/10.1136/ard.2006.062901
  • 25. McNearney TA, Reveille JD, Fischbach M, et al. Pulmonary involvement in systemic sclerosis: associations with genetic, serologic, sociodemographic, and behavioral factors. Arthritis Rheum 2007;57:318-326. https://doi.org/10.1002/art.22532
  • 26. Markusse IM, Meijs J, de Boer B, et al. Predicting cardiopulmonary involvement in patients with systemic sclerosis: complementary value of nailfold videocapillaroscopy patterns and disease-specific autoantibodies. Rheumatology (Oxford) 2017;56:1081-1088. https://doi.org/10.1093/rheumatology/kew402
  • 27. Jung E, Suh CH, Kim HA, Jung JY. Clinical characteristics of systemic sclerosis with ınterstitial lung disease. Arch Rheumatol 2018;33:322-327. https://doi.org/10.5606/ArchRheumatol.2018.6630
  • 28. Ashmore P, Tikly M, Wong M, Ickinger C. Interstitial lung disease in South Africans with systemic sclerosis. Rheumatol Int 2018;38:657-662. https://doi.org/10.1007/s00296-017-3893-0
  • 29. Wangkaew S, Euathrongchit J, Wattanawittawas P, Kasitanon N, Louthrenoo W. Incidence and predictors of interstitial lung disease (ILD) in Thai patients with early systemic sclerosis: inception cohort study. Mod Rheumatol 2016;26:588-593. https://doi.org/10.3109/14397595.2015.1115455
  • 30. Ho KT, Reveille JD. The clinical relevance of autoantibodies in scleroderma. Arthritis Res Ther 2003;5:80-93. https://doi.org/10.1186/ar628
  • 31. Kennedy B, Branagan P, Moloney F, et al. Biomarkers to identify ILD and predict lung function decline in scleroderma lung disease or idiopathic pulmonary fibrosis. Sarcoidosis Vasc Diffuse Lung Dis 2015;32:228-236.
  • 32. Liaskos C, Marou E, Simopoulou T, et al. Disease-related autoantibody profile in patients with systemic sclerosis. Autoimmunity 2017;50:414-421. https://doi.org/10.1080/08916934.2017.1357699
  • 33. Liu X, Mayes MD, Pedroza C, et al. Does C-reactive protein predict the long-term progression of interstitial lung disease and survival in patients with early systemic sclerosis? Arthritis Care Res (Hoboken) 2013;65:1375-1380. https://doi.org/10.1002/acr.21968
  • 34. Mulkoju R, Saka VK, Rajaram M, et al. Pulmonary manifestations in systemic sclerosis: hospital-based descriptive study. Cureus 2020;12:e8649. https://doi.org/10.7759/cureus.8649
  • 35. Avouac J, Airò P, Meune C, et al. Prevalence of pulmonary hypertension in systemic sclerosis in European Caucasians and metaanalysis of 5 studies. J Rheumatol 2010;37:2290-2998. https://doi.org/10.3899/jrheum.100245
  • 36. Erken Pamukcu H, Tunca Ç, Özişler C, et al. Pulmonary hypertension screening in patients with systemic sclerosis, in a tertiary center, in Turkey; a cross-sectional original study. TJCL 2020;11:146-155. https://doi.org/10.18663/tjcl.630633
  • 37. McGoon MD, Benza RL, Escribano Subias P, et al. Pulmonary arterial hypertension: epidemiology and registries. J Am Coll Cardiol 2013;62:51-59. https://doi.org/10.1016/j.jacc.2013.10.023
  • 38. Hachulla E, Launay D. Diagnosis and classification of systemic sclerosis. Clin Rev Allergy Immunol 2011;40:78-83. https://doi.org/10.1007/s12016-010-8198-y
  • 39. Hachulla E, de Groote P, Gressin V, et al. Itinér AIR-Sclérodermie Study Group. The three-year incidence of pulmonary arterial hypertension associated with systemic sclerosis in a multicenter nationwide longitudinal study in France. Arthritis Rheum 2009;60:1831-1839. https://doi.org/10.1002/art.24525
  • 40. Jiang Y, Turk MA, Pope JE. Factors associated with pulmonary arterial hypertension (PAH) in systemic sclerosis (SSc). Autoimmun Rev 2020;19:102602. https://doi.org/10.1016/j.autrev.2020.102602
  • 41. Morrisroe K, Huq M, Stevens W, Rabusa C, Proudman SM, Nikpour M; Australian Scleroderma Interest Group (ASIG). Risk factors for development of pulmonary arterial hypertension in Australian systemic sclerosis patients: results from a large multicenter cohort study. BMC Pulm Med 2016;16:134. https://doi.org/10.1186/s12890-016-0296-z
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Details

Primary Language English
Subjects Rheumatology and Arthritis
Journal Section Research Article
Authors

Tugba Izcı Duran 0000-0003-4428-9873

Melih Pamukcu 0000-0002-9129-0503

Hasan Ulusoy 0000-0001-5463-7363

Early Pub Date June 4, 2024
Publication Date October 9, 2024
Submission Date March 13, 2024
Acceptance Date May 28, 2024
Published in Issue Year 2024

Cite

AMA Izcı Duran T, Pamukcu M, Ulusoy H. Risk factors and biomarkers for ınterstitial lung disease and pulmonary arterial hypertension in systemic sclerosis: experience of two tertiary centers in Türkiye. Pam Tıp Derg. October 2024;17(4):722-731. doi:10.31362/patd.1452076
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