Development and validation of a prognostic model for connective tissue disease-associated interstitial lung disease complicated with pulmonary hypertension_Chinese Journal of Respiratory and Critical Care Medicine

Authors：

FAN Mingwei , JIANG Tianci , LI Pengfei , WANG Yu , ZHAO Wenjing , WU Ruhao , TIAN Xiaoying , ZHANG Mengting ,  CHENG Zhe

Department of Respiratory and Critical Care Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, Henan 450052, P. R. China;

Corresponding author：

CHENG Zhe, Email: fccchengzhe@zzu.edu.cn

Keywords：

Pulmonary hypertension; connective tissue diseases; interstitial lung disease; prognostic model

DOI：

10.7507/1671-6205.202312006

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To investigate independent prognostic factors influencing the prognosis of connective tissue disease-associated interstitial lung disease with pulmonary hypertension (CTD-ILD-PH), and construct a nomogram model using machine learning to predict 1-, 3- and 5-year mortality risks, providing evidence for clinical diagnosis and treatment. Methods Patients diagnosed with CTD-ILD-PH and treated at the First Affiliated Hospital of Zhengzhou University from February 2011 to June 2021 were screened. The least absolute shrinkage and selection operator (Lasso), univariate Cox regression, and multivariate Cox regression analyses were combined to identify independent prognostic factors for CTD-ILD-PH patients. A novel nomogram prognostic model was constructed and internally validated using 1000 bootstrap resamples. The receiver operating characteristic (ROC) curve and Harrell's C-index assessed the predictive performance of the model. Calibration curves evaluated the model fit. Decision curve analysis (DCA) assessed the clinical utility of the model, and external validation was conducted using a separate test set. Results The study included 313 patients, with 108 deaths observed during the follow-up. Using the Lasso-Cox method, albumin, alanine aminotransferase (ALT), red cell volume distribution width (RDW), age, smoking history, rural residence, and pulmonary artery systolic pressure were identified as independent prognostic factors. The Harrell's C-index in the training set was 0.802, and the area under ROC curve was 0.880 (95%CI 0.833 - 0.928). Internal validation showed an average Harrell's C-index of 0.791. Calibration curves indicated high consistency between predicted and observed results. DCA confirmed the model's good clinical utility. External validation results demonstrated the model's favorable predictive performance and clinical utility. Conclusions Our research suggest that lower albumin, elevated ALT, elevated RDW, advanced age, smoking history, rural areas and higher pulmonary artery systolic blood pressure are independent prognostic risk factors for patients with CTD-ILD-PH. In this study, a prognostic model was developed for the first time to predict 1-, 3- and 5-year mortality in CTD-ILD-PH patients, which provides some reference value for future mortality risk assessment in CTD-ILD-PH.

Citation： FAN Mingwei, JIANG Tianci, LI Pengfei, WANG Yu, ZHAO Wenjing, WU Ruhao, TIAN Xiaoying, ZHANG Mengting, CHENG Zhe. Development and validation of a prognostic model for connective tissue disease-associated interstitial lung disease complicated with pulmonary hypertension. Chinese Journal of Respiratory and Critical Care Medicine, 2024, 23(9): 640-650. doi: 10.7507/1671-6205.202312006 Copy

1.	Hao Y, Hudson M, Baron M, et al. Early Mortality in a multinational systemic sclerosis inception cohort. Arthritis Rheumatol, 2017, 69(5): 1067-1077.
2.	Limaye V, Hakendorf P, Woodman RJ, et al. Mortality and its predominant causes in a large cohort of patients with biopsy-determined inflammatory myositis. Intern Med J, 2012, 42(2): 191-198.
3.	Mcgoon M, Gutterman D, Steen V, et al. Screening, early detection, and diagnosis of pulmonary arterial hypertension: ACCP evidence-based clinical practice guidelines. Chest, 2004, 126(1 Suppl): 14s-34s.
4.	Strange C, Highland KB. Pulmonary hypertension in interstitial lung disease. Curr Opin Pulm Med, 2005, 11(5): 452-455.
5.	Behr J, Ryu JH. Pulmonary hypertension in interstitial lung disease. Eur Respir J, 2008, 31(6): 1357-1367.
6.	Zubairi ABS, Ahmad H, Hassan M, et al. Clinical characteristics and factors associated with mortality in idiopathic pulmonary fibrosis: An experience from a tertiary care center in Pakistan. Clin Respir J, 2018, 12(3): 1191-1196.
7.	Michelfelder M, Becker M, Riedlinger A, et al. Interstitial lung disease increases mortality in systemic sclerosis patients with pulmonary arterial hypertension without affecting hemodynamics and exercise capacity. Clin Rheumatol, 2017, 36(2): 381-390.
8.	赵思萌, 邱立军, 吕慧敏, 等. 肺动脉高压对结缔组织病相关间质性肺病的预测意义. 临床内科杂志, 2019, 36(3): 186-189.
9.	王春华. 结缔组织病合并肺动脉高压的临床研究. 中国医学创新, 2015, 12(15): 67-70.
10.	Petri M, Orbai AM, Alarcón GS, et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum, 2012, 64(8): 2677-2686.
11.	Aletaha D, Neogi T, Silman AJ, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum, 2010, 62(9): 2569-2581.
12.	Vitali C, Bombardieri S, Moutsopoulos HM, et al. Assessment of the European classification criteria for Sjögren's syndrome in a series of clinically defined cases: results of a prospective multicentre study. The European Study Group on Diagnostic Criteria for Sjögren's Syndrome. Ann Rheum Dis, 1996, 55(2): 116-121.
13.	Moll JM, Wright V. New York clinical criteria for ankylosing spondylitis. A statistical evaluation. Ann Rheum Dis, 1973, 32(4): 354-363.
14.	Van Der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum, 1984, 27(4): 361-368.
15.	Van Den Hoogen F, Khanna D, Fransen J, et al. 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis, 2013, 72(11): 1747-1755.
16.	Bohan A, Peter JB. Polymyositis and dermatomyositis (first of two parts). N Engl J Med, 1975, 292(7): 344-347.
17.	Bohan A, Peter JB. Polymyositis and dermatomyositis (second of two parts). N Engl J Med, 1975, 292(8): 403-407.
18.	Sharp GC, Irvin WS, Tan EM, et al. Mixed connective tissue disease-an apparently distinct rheumatic disease syndrome associated with a specific antibody to an extractable nuclear antigen (ENA). Am J Med, 1972, 52(2): 148-159.
19.	Bradley B, Branley HM, Egan JJ, et al. Interstitial lung disease guideline: the British Thoracic Society in collaboration with the Thoracic Society of Australia and New Zealand and the Irish Thoracic Society. Thorax, 2008, 63 Suppl 5: v1-v58.
20.	Galiè N, Humbert M, Vachiery JL, et al. 2015 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: The Joint Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS): Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC), International Society for Heart and Lung Transplantation (ISHLT). Eur Respir J, 2015, 46(4): 903-975.
21.	Simonneau G, Montani D, Celermajer DS, et al. Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur Respir J, 2019, 53(1): 1801913.
22.	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(1): 2200879.
23.	Ha YJ, Hur J, Go DJ, et al. Baseline peripheral blood neutrophil-to-lymphocyte ratio could predict survival in patients with adult polymyositis and dermatomyositis: a retrospective observational study. PLoS One, 2018, 13(1): e0190411.
24.	Ballmer PE. Causes and mechanisms of hypoalbuminaemia. Clin Nutr, 2001, 20(3): 271-273.
25.	Snipelisky D, Jentzer J, Batal O, et al. Serum albumin concentration as an independent prognostic indicator in patients with pulmonary arterial hypertension. Clin Cardiol, 2018, 41(6): 782-787.
26.	Kraft SA, Fujishima S, Mcguire GP, et al. Effect of blood and albumin on pulmonary hypertension and edema in perfused rabbit lungs. J Appl Physiol (1985), 1995, 78(2): 499-504.
27.	Botros M, Sikaris KA. The de ritis ratio: the test of time. Clin Biochem Rev, 2013, 34(3): 117-130.
28.	Yogeswaran A, Tello K, Lund J, et al. Risk assessment in pulmonary hypertension based on routinely measured laboratory parameters. J Heart Lung Transplant, 2022, 41(3): 400-410.
29.	Dufour DR, Lott JA, Nolte FS, et al. Diagnosis and monitoring of hepatic injury. I. Performance characteristics of laboratory tests. Clin Chem, 2000, 46(12): 2027-2049.
30.	Subhashree AR, Shanthi B, Parameaswari PJ. The red cell distribution width as a sensitive biomarker for assessing the pulmonary function in automobile welders- a cross sectional study. J Clin Diagn Res, 2013, 7(1): 89-92.
31.	Rhodes CJ, Wharton J, Howard LS, et al. Red cell distribution width outperforms other potential circulating biomarkers in predicting survival in idiopathic pulmonary arterial hypertension. Heart, 2011, 97(13): 1054-1060.
32.	Hampole CV, Mehrotra AK, Thenappan T, et al. Usefulness of red cell distribution width as a prognostic marker in pulmonary hypertension. Am J Cardiol, 2009, 104(6): 868-872.
33.	Rezende SM, Lijfering WM, Rosendaal FR, et al. Hematologic variables and venous thrombosis: red cell distribution width and blood monocyte count are associated with an increased risk. Haematologica, 2014, 99(1): 194-200.
34.	Yu F, Chen H, Li Q, et al. Secular trend of mortality and incidence of rheumatoid arthritis in global , 1990-2019: an age period cohort analysis and joinpoint analysis. BMC Pulm Med, 2023, 23(1): 356.
35.	Kam MLW, Li HH, Tan YH, et al. Validation of the ILD-GAP Model and a Local Nomogram in a Singaporean Cohort. Respiration, 2019, 98(5): 383-390.
36.	Csiszar A, Wang M, Lakatta EG, et al. Inflammation and endothelial dysfunction during aging: role of NF-kappaB. J Appl Physiol (1985), 2008, 105(4): 1333-1341.
37.	Alqarni AA, Brand OJ, Pasini A, et al. Imbalanced prostanoid release mediates cigarette smoke-induced human pulmonary artery cell proliferation. Respir Res, 2022, 23(1): 136.
38.	Berry B, Wright JL. Long-term pulmonary hypertension produced by cigarette smoking is associated with subendocardial fibrosis and inflammation of the right ventricle: a morphometric analysis in the guinea pig model. Exp Pathol, 1991, 43(3-4): 163-172.
39.	Fried ND, Morris TM, Whitehead A, et al. Angiotensin II type 1 receptor mediates pulmonary hypertension and right ventricular remodeling induced by inhaled nicotine. Am J Physiol Heart Circ Physiol, 2021, 320(4): H1526-h1534.
40.	Lee JH, Lee DS, Kim EK, et al. Simvastatin inhibits cigarette smoking-induced emphysema and pulmonary hypertension in rat lungs. Am J Respir Crit Care Med, 2005, 172(8): 987-993.
41.	Wright JL, Levy RD, Churg A. Pulmonary hypertension in chronic obstructive pulmonary disease: current theories of pathogenesis and their implications for treatment. Thorax, 2005, 60(7): 605-609.
42.	Weissmann N, Grimminger F, Seeger W. Smoking: Is it a risk factor for pulmonary vascular diseases? Pulm Circ, 2012, 2(4): 395-396.
43.	Naing P, Kangaharan N, Scalia GM, et al. Pulmonary hypertension in remote and disadvantaged population: overcoming unique challenges for improved outcomes. Intern Med J, 2023, 53(1): 12-20.
44.	Macías CG, Wharam JF, Maron BA, et al. Urban-rural disparities in pulmonary hypertension mortality. Ann Am Thorac Soc, 2020, 17(9): 1168-1171.
45.	Garcia MC, Faul M, Massetti G, et al. Reducing potentially excess deaths from the five leading causes of death in the rural United States. MMWR Surveill Summ, 2017, 66(2): 1-7.
46.	Dai LL, Jiang TC, Li PF, et al. Predictors of maternal death among women with pulmonary hypertension in China from 2012 to 2020: a retrospective single-center study. Front Cardiovasc Med, 2022, 9: 814557.
47.	Lakshmanan S, Jankowich M, Wu WC, et al. Gender differences in risk factors associated with pulmonary artery systolic pressure, heart failure, and mortality in blacks: Jackson Heart Study. J Am Heart Assoc, 2020, 9(1): e013034.
48.	Vonk Noordegraaf A, Westerhof BE, Westerhof N. The relationship between the right ventricle and its load in pulmonary hypertension. J Am Coll Cardiol, 2017, 69(2): 236-243.
49.	Klinger JR. Group III pulmonary hypertension: pulmonary hypertension associated with lung disease: epidemiology, pathophysiology, and treatments. Cardiol Clin, 2016, 34(3): 413-433.
50.	Riepl G. Effects of abnormal hemoglobin concentration in human blood on membrane diffusing capacity of the lung and on pulmonary capillary blood volume. Respiration, 1978, 36(1): 10-18.
51.	Priel E, Diab N, Patel M, et al. The added value of haemoglobin to height, age, and sex to predict D_LCO in subjects with preserved exercise capacity. PLoS One, 2023, 18(8): e0289540.
52.	Nakade Y, Toyama T, Furuichi K, et al. Impact of kidney function and urinary protein excretion on pulmonary function in Japanese patients with chronic kidney disease. Clin Exp Nephrol, 2014, 18(5): 763-769.

1. Hao Y, Hudson M, Baron M, et al. Early Mortality in a multinational systemic sclerosis inception cohort. Arthritis Rheumatol, 2017, 69(5): 1067-1077.
2. Limaye V, Hakendorf P, Woodman RJ, et al. Mortality and its predominant causes in a large cohort of patients with biopsy-determined inflammatory myositis. Intern Med J, 2012, 42(2): 191-198.
3. Mcgoon M, Gutterman D, Steen V, et al. Screening, early detection, and diagnosis of pulmonary arterial hypertension: ACCP evidence-based clinical practice guidelines. Chest, 2004, 126(1 Suppl): 14s-34s.
4. Strange C, Highland KB. Pulmonary hypertension in interstitial lung disease. Curr Opin Pulm Med, 2005, 11(5): 452-455.
5. Behr J, Ryu JH. Pulmonary hypertension in interstitial lung disease. Eur Respir J, 2008, 31(6): 1357-1367.
6. Zubairi ABS, Ahmad H, Hassan M, et al. Clinical characteristics and factors associated with mortality in idiopathic pulmonary fibrosis: An experience from a tertiary care center in Pakistan. Clin Respir J, 2018, 12(3): 1191-1196.
7. Michelfelder M, Becker M, Riedlinger A, et al. Interstitial lung disease increases mortality in systemic sclerosis patients with pulmonary arterial hypertension without affecting hemodynamics and exercise capacity. Clin Rheumatol, 2017, 36(2): 381-390.
8. 赵思萌, 邱立军, 吕慧敏, 等. 肺动脉高压对结缔组织病相关间质性肺病的预测意义. 临床内科杂志, 2019, 36(3): 186-189.
9. 王春华. 结缔组织病合并肺动脉高压的临床研究. 中国医学创新, 2015, 12(15): 67-70.
10. Petri M, Orbai AM, Alarcón GS, et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum, 2012, 64(8): 2677-2686.
11. Aletaha D, Neogi T, Silman AJ, et al. 2010 Rheumatoid arthritis classification criteria: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Arthritis Rheum, 2010, 62(9): 2569-2581.
12. Vitali C, Bombardieri S, Moutsopoulos HM, et al. Assessment of the European classification criteria for Sjögren's syndrome in a series of clinically defined cases: results of a prospective multicentre study. The European Study Group on Diagnostic Criteria for Sjögren's Syndrome. Ann Rheum Dis, 1996, 55(2): 116-121.
13. Moll JM, Wright V. New York clinical criteria for ankylosing spondylitis. A statistical evaluation. Ann Rheum Dis, 1973, 32(4): 354-363.
14. Van Der Linden S, Valkenburg HA, Cats A. Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum, 1984, 27(4): 361-368.
15. Van Den Hoogen F, Khanna D, Fransen J, et al. 2013 classification criteria for systemic sclerosis: an American college of rheumatology/European league against rheumatism collaborative initiative. Ann Rheum Dis, 2013, 72(11): 1747-1755.
16. Bohan A, Peter JB. Polymyositis and dermatomyositis (first of two parts). N Engl J Med, 1975, 292(7): 344-347.
17. Bohan A, Peter JB. Polymyositis and dermatomyositis (second of two parts). N Engl J Med, 1975, 292(8): 403-407.
18. Sharp GC, Irvin WS, Tan EM, et al. Mixed connective tissue disease-an apparently distinct rheumatic disease syndrome associated with a specific antibody to an extractable nuclear antigen (ENA). Am J Med, 1972, 52(2): 148-159.
19. Bradley B, Branley HM, Egan JJ, et al. Interstitial lung disease guideline: the British Thoracic Society in collaboration with the Thoracic Society of Australia and New Zealand and the Irish Thoracic Society. Thorax, 2008, 63 Suppl 5: v1-v58.
20. Galiè N, Humbert M, Vachiery JL, et al. 2015 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension: The Joint Task Force for the Diagnosis and Treatment of Pulmonary Hypertension of the European Society of Cardiology (ESC) and the European Respiratory Society (ERS): Endorsed by: Association for European Paediatric and Congenital Cardiology (AEPC), International Society for Heart and Lung Transplantation (ISHLT). Eur Respir J, 2015, 46(4): 903-975.
21. Simonneau G, Montani D, Celermajer DS, et al. Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur Respir J, 2019, 53(1): 1801913.
22. 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(1): 2200879.
23. Ha YJ, Hur J, Go DJ, et al. Baseline peripheral blood neutrophil-to-lymphocyte ratio could predict survival in patients with adult polymyositis and dermatomyositis: a retrospective observational study. PLoS One, 2018, 13(1): e0190411.
24. Ballmer PE. Causes and mechanisms of hypoalbuminaemia. Clin Nutr, 2001, 20(3): 271-273.
25. Snipelisky D, Jentzer J, Batal O, et al. Serum albumin concentration as an independent prognostic indicator in patients with pulmonary arterial hypertension. Clin Cardiol, 2018, 41(6): 782-787.
26. Kraft SA, Fujishima S, Mcguire GP, et al. Effect of blood and albumin on pulmonary hypertension and edema in perfused rabbit lungs. J Appl Physiol (1985), 1995, 78(2): 499-504.
27. Botros M, Sikaris KA. The de ritis ratio: the test of time. Clin Biochem Rev, 2013, 34(3): 117-130.
28. Yogeswaran A, Tello K, Lund J, et al. Risk assessment in pulmonary hypertension based on routinely measured laboratory parameters. J Heart Lung Transplant, 2022, 41(3): 400-410.
29. Dufour DR, Lott JA, Nolte FS, et al. Diagnosis and monitoring of hepatic injury. I. Performance characteristics of laboratory tests. Clin Chem, 2000, 46(12): 2027-2049.
30. Subhashree AR, Shanthi B, Parameaswari PJ. The red cell distribution width as a sensitive biomarker for assessing the pulmonary function in automobile welders- a cross sectional study. J Clin Diagn Res, 2013, 7(1): 89-92.
31. Rhodes CJ, Wharton J, Howard LS, et al. Red cell distribution width outperforms other potential circulating biomarkers in predicting survival in idiopathic pulmonary arterial hypertension. Heart, 2011, 97(13): 1054-1060.
32. Hampole CV, Mehrotra AK, Thenappan T, et al. Usefulness of red cell distribution width as a prognostic marker in pulmonary hypertension. Am J Cardiol, 2009, 104(6): 868-872.
33. Rezende SM, Lijfering WM, Rosendaal FR, et al. Hematologic variables and venous thrombosis: red cell distribution width and blood monocyte count are associated with an increased risk. Haematologica, 2014, 99(1): 194-200.
34. Yu F, Chen H, Li Q, et al. Secular trend of mortality and incidence of rheumatoid arthritis in global , 1990-2019: an age period cohort analysis and joinpoint analysis. BMC Pulm Med, 2023, 23(1): 356.
35. Kam MLW, Li HH, Tan YH, et al. Validation of the ILD-GAP Model and a Local Nomogram in a Singaporean Cohort. Respiration, 2019, 98(5): 383-390.
36. Csiszar A, Wang M, Lakatta EG, et al. Inflammation and endothelial dysfunction during aging: role of NF-kappaB. J Appl Physiol (1985), 2008, 105(4): 1333-1341.
37. Alqarni AA, Brand OJ, Pasini A, et al. Imbalanced prostanoid release mediates cigarette smoke-induced human pulmonary artery cell proliferation. Respir Res, 2022, 23(1): 136.
38. Berry B, Wright JL. Long-term pulmonary hypertension produced by cigarette smoking is associated with subendocardial fibrosis and inflammation of the right ventricle: a morphometric analysis in the guinea pig model. Exp Pathol, 1991, 43(3-4): 163-172.
39. Fried ND, Morris TM, Whitehead A, et al. Angiotensin II type 1 receptor mediates pulmonary hypertension and right ventricular remodeling induced by inhaled nicotine. Am J Physiol Heart Circ Physiol, 2021, 320(4): H1526-h1534.
40. Lee JH, Lee DS, Kim EK, et al. Simvastatin inhibits cigarette smoking-induced emphysema and pulmonary hypertension in rat lungs. Am J Respir Crit Care Med, 2005, 172(8): 987-993.
41. Wright JL, Levy RD, Churg A. Pulmonary hypertension in chronic obstructive pulmonary disease: current theories of pathogenesis and their implications for treatment. Thorax, 2005, 60(7): 605-609.
42. Weissmann N, Grimminger F, Seeger W. Smoking: Is it a risk factor for pulmonary vascular diseases? Pulm Circ, 2012, 2(4): 395-396.
43. Naing P, Kangaharan N, Scalia GM, et al. Pulmonary hypertension in remote and disadvantaged population: overcoming unique challenges for improved outcomes. Intern Med J, 2023, 53(1): 12-20.
44. Macías CG, Wharam JF, Maron BA, et al. Urban-rural disparities in pulmonary hypertension mortality. Ann Am Thorac Soc, 2020, 17(9): 1168-1171.
45. Garcia MC, Faul M, Massetti G, et al. Reducing potentially excess deaths from the five leading causes of death in the rural United States. MMWR Surveill Summ, 2017, 66(2): 1-7.
46. Dai LL, Jiang TC, Li PF, et al. Predictors of maternal death among women with pulmonary hypertension in China from 2012 to 2020: a retrospective single-center study. Front Cardiovasc Med, 2022, 9: 814557.
47. Lakshmanan S, Jankowich M, Wu WC, et al. Gender differences in risk factors associated with pulmonary artery systolic pressure, heart failure, and mortality in blacks: Jackson Heart Study. J Am Heart Assoc, 2020, 9(1): e013034.
48. Vonk Noordegraaf A, Westerhof BE, Westerhof N. The relationship between the right ventricle and its load in pulmonary hypertension. J Am Coll Cardiol, 2017, 69(2): 236-243.
49. Klinger JR. Group III pulmonary hypertension: pulmonary hypertension associated with lung disease: epidemiology, pathophysiology, and treatments. Cardiol Clin, 2016, 34(3): 413-433.
50. Riepl G. Effects of abnormal hemoglobin concentration in human blood on membrane diffusing capacity of the lung and on pulmonary capillary blood volume. Respiration, 1978, 36(1): 10-18.
51. Priel E, Diab N, Patel M, et al. The added value of haemoglobin to height, age, and sex to predict D_LCO in subjects with preserved exercise capacity. PLoS One, 2023, 18(8): e0289540.
52. Nakade Y, Toyama T, Furuichi K, et al. Impact of kidney function and urinary protein excretion on pulmonary function in Japanese patients with chronic kidney disease. Clin Exp Nephrol, 2014, 18(5): 763-769.

Chinese Journal of Respiratory and Critical Care Medicine

Development and validation of a prognostic model for connective tissue disease-associated interstitial lung disease complicated with pulmonary hypertension

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content