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Current Vascular Pharmacology

Editor-in-Chief

ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

Research Article

Diagnostic Value of Serum Galectin-3 Binding Protein Level in Patients with Pulmonary Arterial Hypertension

Author(s): Mingfei Li, Wenzhi Pan, Dan Tian, Dandan Chen, Xiaochun Zhang, Yuan Zhang, Shasha Chen, Daxin Zhou* and Junbo Ge*

Volume 22, Issue 1, 2024

Published on: 01 December, 2023

Page: [67 - 77] Pages: 11

DOI: 10.2174/0115701611268078231010072521

Price: $65

Abstract

Background: Pulmonary arterial hypertension (PAH) still lacks effective biomarkers to assist in its diagnosis and prognosis. Galectin-3 binding protein (Gal-3BP) plays a role in immune and inflammatory diseases.

Objective: This study aimed to evaluate Gal-3BP as a prognostic and predictive factor in patients with PAH.

Methods: From January 2017 to December 2019, we enrolled 167 consecutive PAH patients and 58 healthy controls. Right heart catheterization (RHC) was used to diagnose PAH. Serum Gal-3BP levels were measured by high-sensitivity human enzyme-linked immunosorbent assay (ELISA).

Results: Serum Gal-3BP levels in the PAH group were significantly higher compared with the control group (4.87±2.09 vs 2.22±0.86 μg/mL, p<0.001). Gal-3BP level was correlated with several hemodynamic parameters obtained from RHC (p<0.001). Multivariate linear regression analysis showed that Gal-3BP was a risk factor for PAH (odds ratio (OR)=2.947, 95% CI: 1.821-4.767, p<0.001). The optimal cut-off value of serum Gal-3BP level for predicting PAH was 2.89 μg/mL (area under the curve (AUC)=0.860, 95 % CI: 0.811-0.910, p<0.001). Kaplan-Meier analysis showed that Gal-3BP levels above the median (4.87 μg/mL) were associated with an increased risk of death in patients with PAH (hazard ratio (HR)=8.868, 95 % CI: 3.631-21.65, p<0.0001). Cox multivariate risk regression analysis showed that Gal-3BP was a risk factor for death in PAH patients (HR=2.779, 95 % CI: 1.823-4.237, p<0.001).

Conclusion: Serum Gal-3BP levels were increased in patients with PAH, and levels of Gal-3BP were associated with the severity of PAH. Gal-3BP might have predictive value for the diagnosis and prognosis of PAH.

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[1]
Humbert M, Kovacs G, Hoeper MM, et al. 2022 ESC/ERS Guidelines for the diagnosis and treatment of pulmonary hypertension. Eur Heart J 2022; 43(38): 3618-731.
[http://dx.doi.org/10.1093/eurheartj/ehac237] [PMID: 36017548]
[2]
Rosenzweig EB, Abman SH, Adatia I, et al. Paediatric pulmonary arterial hypertension: updates on definition, classification, diagnostics and management. Eur Respir J 2019; 53(1): 1801916.
[http://dx.doi.org/10.1183/13993003.01916-2018] [PMID: 30545978]
[3]
Hoeper MM, Humbert M, Souza R, et al. A global view of pulmonary hypertension. Lancet Respir Med 2016; 4(4): 306-22.
[http://dx.doi.org/10.1016/S2213-2600(15)00543-3] [PMID: 26975810]
[4]
Fukuda K, Date H, Doi S, et al. Guidelines for the treatment of pulmonary hypertension (jcs 2017/jpcphs 2017). Circ J 2019; 83(4): 842-945.
[http://dx.doi.org/10.1253/circj.CJ-66-0158] [PMID: 30853682]
[5]
Park JH, Na JO, Lee JS, Kim YH, Chang HJ. 2020 KSC/KATRD Guideline for the Diagnosis and Treatment of Pulmonary Hypertension: Executive Summary. Tuberc Respir Dis 2022; 85(1): 1-10.
[http://dx.doi.org/10.4046/trd.2021.0022] [PMID: 34134466]
[6]
Simonneau G, Montani D, Celermajer DS, et al. Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur Respir J 2019; 53(1): 1801913.
[http://dx.doi.org/10.1183/13993003.01913-2018] [PMID: 30545968]
[7]
Frump AL, Bonnet S, de Jesus Perez VA, Lahm T. Emerging role of angiogenesis in adaptive and maladaptive right ventricular remodeling in pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2018; 314(3): L443-60.
[http://dx.doi.org/10.1152/ajplung.00374.2017] [PMID: 29097426]
[8]
D’Alonzo GE, Barst RJ, Ayres SM, et al. Survival in patients with primary pulmonary hypertension. Results from a national prospective registry. Ann Intern Med 1991; 115(5): 343-9.
[http://dx.doi.org/10.7326/0003-4819-115-5-343] [PMID: 1863023]
[9]
Stubbs H, Johnson M. Pulmonary hypertension for the non-specialist. J R Coll Phys Edinb 2021; 51(4): 392-401.
[http://dx.doi.org/10.4997/jrcpe.2021.419] [PMID: 34882144]
[10]
Farber HW, Miller DP, Poms AD, et al. Five-Year outcomes of patients enrolled in the REVEAL registry. Chest 2015; 148(4): 1043-54.
[http://dx.doi.org/10.1378/chest.15-0300] [PMID: 26066077]
[11]
Badesch DB, Raskob GE, Elliott CG, et al. Pulmonary arterial hypertension: baseline characteristics from the REVEAL registry. Chest 2010; 137(2): 376-87.
[http://dx.doi.org/10.1378/chest.09-1140] [PMID: 19837821]
[12]
Wilkins MR. Pulmonary hypertension: the science behind the disease spectrum. Eur Respir Rev 2012; 21(123): 19-26.
[http://dx.doi.org/10.1183/09059180.00008411] [PMID: 22379170]
[13]
Bjornsson J, Edwards WD. Primary pulmonary hypertension: A histopathologic study of 80 cases. Mayo Clin Proc 1985; 60(1): 16-25.
[http://dx.doi.org/10.1016/S0025-6196(12)65277-X] [PMID: 3965821]
[14]
Marsboom G, Toth PT, Ryan JJ, et al. Dynamin-related protein 1-mediated mitochondrial mitotic fission permits hyperproliferation of vascular smooth muscle cells and offers a novel therapeutic target in pulmonary hypertension. Circ Res 2012; 110(11): 1484-97.
[http://dx.doi.org/10.1161/CIRCRESAHA.111.263848] [PMID: 22511751]
[15]
Bonnet S, Michelakis ED, Porter CJ, et al. An abnormal mitochondrial-hypoxia inducible factor-1alpha-Kv channel pathway disrupts oxygen sensing and triggers pulmonary arterial hypertension in fawn hooded rats: similarities to human pulmonary arterial hypertension. Circulation 2006; 113(22): 2630-41.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.105.609008] [PMID: 16735674]
[16]
Diebold I, Hennigs JK, Miyagawa K, et al. BMPR2 preserves mitochondrial function and DNA during reoxygenation to promote endothelial cell survival and reverse pulmonary hypertension. Cell Metab 2015; 21(4): 596-608.
[http://dx.doi.org/10.1016/j.cmet.2015.03.010] [PMID: 25863249]
[17]
Archer SL, Marsboom G, Kim GH, et al. Epigenetic attenuation of mitochondrial superoxide dismutase 2 in pulmonary arterial hypertension: a basis for excessive cell proliferation and a new therapeutic target. Circulation 2010; 121(24): 2661-71.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.109.916098] [PMID: 20529999]
[18]
Joshi SR, Kitagawa A, Jacob C, et al. Hypoxic activation of glucose-6-phosphate dehydrogenase controls the expression of genes involved in the pathogenesis of pulmonary hypertension through the regulation of DNA methylation. Am J Physiol Lung Cell Mol Physiol 2020; 318(4): L773-86.
[http://dx.doi.org/10.1152/ajplung.00001.2020] [PMID: 32159369]
[19]
Yan Y, He YY, Jiang X, et al. DNA methyltransferase 3B deficiency unveils a new pathological mechanism of pulmonary hypertension. Sci Adv 2020; 6(50): eaba2470.
[http://dx.doi.org/10.1126/sciadv.aba2470] [PMID: 33298433]
[20]
Zhao L, Chen CN, Hajji N, et al. Histone deacetylation inhibition in pulmonary hypertension: therapeutic potential of valproic acid and suberoylanilide hydroxamic acid. Circulation 2012; 126(4): 455-67.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.112.103176] [PMID: 22711276]
[21]
Chelladurai P, Boucherat O, Stenmark K, et al. Targeting histone acetylation in pulmonary hypertension and right ventricular hypertrophy. Br J Pharmacol 2021; 178(1): 54-71.
[http://dx.doi.org/10.1111/bph.14932] [PMID: 31749139]
[22]
Caruso P, Dempsie Y, Stevens HC, et al. A role for miR-145 in pulmonary arterial hypertension: Evidence from mouse models and patient samples. Circ Res 2012; 111(3): 290-300.
[http://dx.doi.org/10.1161/CIRCRESAHA.112.267591] [PMID: 22715469]
[23]
Kim J, Kang Y, Kojima Y, et al. An endothelial apelin-FGF link mediated by miR-424 and miR-503 is disrupted in pulmonary arterial hypertension. Nat Med 2013; 19(1): 74-82.
[http://dx.doi.org/10.1038/nm.3040] [PMID: 23263626]
[24]
Ali MK, Schimmel K, Zhao L, et al. The role of circular RNAs in pulmonary hypertension. Eur Respir J 2022; 60(6): 2200012.
[http://dx.doi.org/10.1183/13993003.00012-2022] [PMID: 35680145]
[25]
Meloche J, Paulin R, Provencher S, Bonnet S. Therapeutic potential of microrna modulation in pulmonary arterial hypertension. Curr Vasc Pharmacol 2015; 13(3): 331-40.
[http://dx.doi.org/10.2174/15701611113119990010] [PMID: 23713859]
[26]
Gorelova A, Berman M, Al Ghouleh I. Endothelial-to-Mesenchymal transition in pulmonary arterial hypertension. Antioxid Redox Signal 2021; 34(12): 891-914.
[http://dx.doi.org/10.1089/ars.2020.8169] [PMID: 32746619]
[27]
Ni S, Ji T, Dong J, et al. Immune cells in pulmonary arterial hypertension. Heart Lung Circ 2022; 31(7): 934-43.
[http://dx.doi.org/10.1016/j.hlc.2022.02.007] [PMID: 35361533]
[28]
Frid MG, McKeon BA, Thurman JM, et al. Immunoglobulin-driven complement activation regulates proinflammatory remodeling in pulmonary hypertension. Am J Respir Crit Care Med 2020; 201(2): 224-39.
[http://dx.doi.org/10.1164/rccm.201903-0591OC] [PMID: 31545648]
[29]
Soon E, Holmes AM, Treacy CM, et al. Elevated levels of inflammatory cytokines predict survival in idiopathic and familial pulmonary arterial hypertension. Circulation 2010; 122(9): 920-7.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.109.933762] [PMID: 20713898]
[30]
Wang R, Yuan T, Wang J, et al. Immunity and inflammation in pulmonary arterial hypertension: From pathophysiology mechanisms to treatment perspective. Pharmacol Res 2022; 180: 106238.
[http://dx.doi.org/10.1016/j.phrs.2022.106238] [PMID: 35504356]
[31]
Mercurio V, Cuomo A, Naranjo M, Hassoun PM. Inflammatory mechanisms in the pathogenesis of pulmonary arterial hypertension: recent advances. Compr Physiol 2021; 11(2): 1805-29.
[http://dx.doi.org/10.1002/cphy.c200025] [PMID: 33792903]
[32]
Kherbeck N, Tamby MC, Bussone G, et al. The role of inflammation and autoimmunity in the pathophysiology of pulmonary arterial hypertension. Clin Rev Allergy Immunol 2013; 44(1): 31-8.
[http://dx.doi.org/10.1007/s12016-011-8265-z] [PMID: 21394427]
[33]
Tang C, Luo Y, Li S, Huang B, Xu S, Li L. Characteristics of inflammation process in monocrotaline-induced pulmonary arterial hypertension in rats. Biomed Pharmacother 2021; 133: 111081.
[http://dx.doi.org/10.1016/j.biopha.2020.111081] [PMID: 33378977]
[34]
Hu Y, Chi L, Kuebler WM, Goldenberg NM. Perivascular inflammation in pulmonary arterial hypertension. Cells 2020; 9(11): 2338.
[http://dx.doi.org/10.3390/cells9112338] [PMID: 33105588]
[35]
Loimaranta V, Hepojoki J, Laaksoaho O, Pulliainen AT. Galectin-3-binding protein: A multitask glycoprotein with innate immunity functions in viral and bacterial infections. J Leukoc Biol 2018; 104(4): 777-86.
[http://dx.doi.org/10.1002/JLB.3VMR0118-036R] [PMID: 29882603]
[36]
Martínez VG, Moestrup SK, Holmskov U, Mollenhauer J, Lozano F. The conserved scavenger receptor cysteine-rich superfamily in therapy and diagnosis. Pharmacol Rev 2011; 63(4): 967-1000.
[http://dx.doi.org/10.1124/pr.111.004523] [PMID: 21880988]
[37]
Hohenester E, Sasaki T, Timpl R. Crystal structure of a scavenger receptor cysteine-rich domain sheds light on an ancient superfamily. Nat Struct Biol 1999; 6(3): 228-32.
[http://dx.doi.org/10.1038/6669] [PMID: 10074941]
[38]
White MJV, Roife D, Gomer RH. Galectin-3 binding protein secreted by breast cancer cells inhibits monocyte-derived fibrocyte differentiation. J Immunol 2015; 195(4): 1858-67.
[http://dx.doi.org/10.4049/jimmunol.1500365] [PMID: 26136428]
[39]
Lin TW, Chang HT, Chen CH, et al. Galectin-3 binding protein and galectin-1 interaction in breast cancer cell aggregation and metastasis. J Am Chem Soc 2015; 137(30): 9685-93.
[http://dx.doi.org/10.1021/jacs.5b04744] [PMID: 26168351]
[40]
Li Y, Komai-Koma M, Gilchrist DS, et al. Galectin-3 is a negative regulator of lipopolysaccharide-mediated inflammation. J Immunol 2008; 181(4): 2781-9.
[http://dx.doi.org/10.4049/jimmunol.181.4.2781] [PMID: 18684969]
[41]
Kim YS, Jung JA, Kim HJ, et al. Galectin-3 binding protein promotes cell motility in colon cancer by stimulating the shedding of protein tyrosine phosphatase kappa by proprotein convertase 5. Biochem Biophys Res Commun 2011; 404(1): 96-102.
[http://dx.doi.org/10.1016/j.bbrc.2010.11.071] [PMID: 21094132]
[42]
Ohshima S, Kuchen S, Seemayer CA, et al. Galectin 3 and its binding protein in rheumatoid arthritis. Arthritis Rheum 2003; 48(10): 2788-95.
[http://dx.doi.org/10.1002/art.11287] [PMID: 14558084]
[43]
Maekawa T, Kamada Y, Ebisutani Y, et al. Serum Mac-2 binding protein is a novel biomarker for chronic pancreatitis. World J Gastroenterol 2016; 22(17): 4403-10.
[http://dx.doi.org/10.3748/wjg.v22.i17.4403] [PMID: 27158210]
[44]
Fukaya Y, Shimada H, Wang LC, Zandi E, DeClerck YA. Identification of galectin-3-binding protein as a factor secreted by tumor cells that stimulates interleukin-6 expression in the bone marrow stroma. J Biol Chem 2008; 283(27): 18573-81.
[http://dx.doi.org/10.1074/jbc.M803115200] [PMID: 18450743]
[45]
Ullrich A, Sures I, D’Egidio M, et al. The secreted tumor-associated antigen 90K is a potent immune stimulator. J Biol Chem 1994; 269(28): 18401-7.
[http://dx.doi.org/10.1016/S0021-9258(17)32322-0] [PMID: 8034587]
[46]
Zhen S, Cai R, Yang X, Ma Y, Wen D. Association of Serum Galectin-3-Binding protein and metabolic syndrome in a chinese adult population. Front Endocrinol 2021; 12: 726154.
[http://dx.doi.org/10.3389/fendo.2021.726154] [PMID: 34858323]
[47]
Sugiura T, Dohi Y, Takase H, et al. Serum levels of Mac-2 binding protein increase with cardiovascular risk and reflect silent atherosclerosis. Atherosclerosis 2016; 251: 192-6.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.06.027] [PMID: 27344370]
[48]
Gleissner CA, Erbel C, Linden F, et al. Galectin-3 binding protein plasma levels are associated with long-term mortality in coronary artery disease independent of plaque morphology. Atherosclerosis 2016; 251: 94-100.
[http://dx.doi.org/10.1016/j.atherosclerosis.2016.06.002] [PMID: 27295060]
[49]
Galiè N, Humbert M, Vachiery JL, et al. 2015 ESC/ERS guidelines for the diagnosis and treatment of pulmonary hypertension. Eur Respir J 2015; 46(4): 903-75.
[http://dx.doi.org/10.1183/13993003.01032-2015] [PMID: 26318161]
[50]
Mares A, Mukherjee D, Lange RA, Nickel NP. Targeted therapies in patients with pulmonary arterial hypertension due to congenital heart disease. Curr Vasc Pharmacol 2022; 20(4): 341-60.
[http://dx.doi.org/10.2174/1570161120666220811150853] [PMID: 36125818]
[51]
Ivy DD, Abman SH, Barst RJ, et al. Pediatric pulmonary hypertension. J Am Coll Cardiol 2013; 62(25) (Suppl.): D117-26.
[http://dx.doi.org/10.1016/j.jacc.2013.10.028] [PMID: 24355636]
[52]
Morrell NW, Aldred MA, Chung WK, et al. Genetics and genomics of pulmonary arterial hypertension. Eur Respir J 2019; 53(1): 1801899.
[http://dx.doi.org/10.1183/13993003.01899-2018] [PMID: 30545973]
[53]
Oliveira AC, Richards EM, Raizada MK. Pulmonary hypertension: Pathophysiology beyond the lung. Pharmacol Res 2020; 151: 104518.
[http://dx.doi.org/10.1016/j.phrs.2019.104518] [PMID: 31730803]
[54]
Pasha MAQ, Newman JH. High-altitude disorders: Pulmonary hypertension: Pulmonary vascular disease: the global perspective. Chest 2010; 137(6) (Suppl.): 13S-9S.
[http://dx.doi.org/10.1378/chest.09-2445] [PMID: 20522576]
[55]
Mocumbi AO, Thienemann F, Sliwa K. A global perspective on the epidemiology of pulmonary hypertension. Can J Cardiol 2015; 31(4): 375-81.
[http://dx.doi.org/10.1016/j.cjca.2015.01.030] [PMID: 25840090]
[56]
Aldred MA, Morrell NW, Guignabert C. New mutations and pathogenesis of pulmonary hypertension: Progress and puzzles in disease pathogenesis. Circ Res 2022; 130(9): 1365-81.
[http://dx.doi.org/10.1161/CIRCRESAHA.122.320084] [PMID: 35482831]
[57]
Dimitroulas T, Giannakoulas G, Karvounis H, Settas L, Kitas GD. Biomarkers in systemic sclerosis-related pulmonary arterial hypertension. Curr Vasc Pharmacol 2011; 9(2): 213-9.
[http://dx.doi.org/10.2174/157016111794519381] [PMID: 21143174]
[58]
Boucly A, Tu L, Guignabert C, et al. Cytokines as prognostic biomarkers in pulmonary arterial hypertension. Eur Respir J 2023; 61(3): 2201232.
[http://dx.doi.org/10.1183/13993003.01232-2022] [PMID: 36549710]
[59]
Coleman RD, Chartan CA, Ivy DD. MicroRNA as a biomarker in pediatric pulmonary hypertension: A step closer to the holy grail? Pediatr Crit Care Med 2020; 21(4): 393-4.
[http://dx.doi.org/10.1097/PCC.0000000000002219] [PMID: 32251186]
[60]
Rhodes CJ, Wharton J, Swietlik EM, et al. Using the plasma proteome for risk stratifying patients with pulmonary arterial hypertension. Am J Respir Crit Care Med 2022; 205(9): 1102-11.
[http://dx.doi.org/10.1164/rccm.202105-1118OC] [PMID: 35081018]
[61]
Xu J, Linneman J, Zhong Y, et al. MicroRNAs in pulmonary hypertension, from pathogenesis to diagnosis and treatment. Biomolecules 2022; 12(4): 496.
[http://dx.doi.org/10.3390/biom12040496] [PMID: 35454085]
[62]
Omura J, Habbout K, Shimauchi T, et al. Identification of long noncoding rna h19 as a new biomarker and therapeutic target in right ventricular failure in pulmonary arterial hypertension. Circulation 2020; 142(15): 1464-84.
[http://dx.doi.org/10.1161/CIRCULATIONAHA.120.047626] [PMID: 32698630]
[63]
Fijalkowska A, Kurzyna M, Torbicki A, et al. Serum N-terminal brain natriuretic peptide as a prognostic parameter in patients with pulmonary hypertension. Chest 2006; 129(5): 1313-21.
[http://dx.doi.org/10.1378/chest.129.5.1313] [PMID: 16685024]
[64]
Keranov S, Dörr O, Jafari L, et al. CILP1 as a biomarker for right ventricular maladaptation in pulmonary hypertension. Eur Respir J 2021; 57(4): 1901192.
[http://dx.doi.org/10.1183/13993003.01192-2019] [PMID: 33184116]
[65]
Llucià-Valldeperas A, van Wezenbeek J, Goumans MJ, de Man FS. The battle of new biomarkers for right heart failure in pulmonary hypertension: Is the queen of hearts NT-proBNP defeated at last? Eur Respir J 2021; 57(4): 2004277.
[http://dx.doi.org/10.1183/13993003.04277-2020] [PMID: 33795356]
[66]
Berghaus TM, Kutsch J, Faul C, von Scheidt W, Schwaiblmair M. The association of N-terminal pro-brain-type natriuretic peptide with hemodynamics and functional capacity in therapy-naive precapillary pulmonary hypertension: results from a cohort study. BMC Pulm Med 2017; 17(1): 167.
[http://dx.doi.org/10.1186/s12890-017-0521-4] [PMID: 29202745]
[67]
Gan CT, McCann GP, Marcus JT, et al. NT-proBNP reflects right ventricular structure and function in pulmonary hypertension. Eur Respir J 2006; 28(6): 1190-4.
[http://dx.doi.org/10.1183/09031936.00016006] [PMID: 16971413]
[68]
Gagno G, Padoan L, Stenner E, et al. Galectin 3 and Galectin 3 binding protein improve the risk stratification after myocardial infarction. J Clin Med 2019; 8(5): 570.
[http://dx.doi.org/10.3390/jcm8050570] [PMID: 31035456]
[69]
Georgoulis M, Mikhailidis DP, Panagiotakos DB. Are serum uric acid levels predictors of cardiovascular risk? An update. Curr Opin Cardiol 2023; 38(4): 337-43.
[http://dx.doi.org/10.1097/HCO.0000000000001029] [PMID: 36789778]
[70]
Hisatome I, Li P, Miake J, et al. Uric acid as a risk factor for chronic kidney disease and cardiovascular disease-Japanese guideline on the management of asymptomatic hyperuricemia. Circ J 2021; 85(2): 130-8.
[http://dx.doi.org/10.1253/circj.CJ-20-0406] [PMID: 33342914]
[71]
Katsiki N, Kouvari M, Panagiotakos DB, et al. The association between serum uric acid levels and 10-year cardiovascular disease incidence: Results from the ATTICA prospective study. Rev Cardiovasc Med 2021; 22(3): 991-1001.
[http://dx.doi.org/10.31083/j.rcm2203108] [PMID: 34565100]
[72]
Nickel NP, O’Leary JM, Brittain EL, et al. Kidney dysfunction in patients with pulmonary arterial hypertension. Pulm Circ 2017; 7(1): 38-54.
[http://dx.doi.org/10.1086/690018] [PMID: 28680564]
[73]
Bitker L, Sens F, Payet C, et al. Presence of kidney disease as an outcome predictor in patients with pulmonary arterial hypertension. Am J Nephrol 2108; 47(2): 134-43.
[http://dx.doi.org/10.1159/000487198]
[74]
Nagaya N, Uematsu M, Satoh T, et al. Serum uric acid levels correlate with the severity and the mortality of primary pulmonary hypertension. Am J Respir Crit Care Med 1999; 160(2): 487-92.
[http://dx.doi.org/10.1164/ajrccm.160.2.9812078] [PMID: 10430718]
[75]
Cerik IB, Dindas F, Koyun E, et al. New prognostic markers in pulmonary arterial hypertension: CRP to albumin ratio and uric acid. Clin Biochem 2022; 100: 22-8.
[http://dx.doi.org/10.1016/j.clinbiochem.2021.11.004] [PMID: 34788635]
[76]
Hanaoka H, Ishigaki S, Takei H, et al. Early combination of pulmonary vasodilators prevents chronic kidney disease progression in connective tissue disease-associated pulmonary hypertension. Int J Rheum Dis 2021; 24(11): 1419-26.
[http://dx.doi.org/10.1111/1756-185X.14225] [PMID: 34626090]
[77]
Gonzalez-Hermosillo LM, Cueto-Robledo G, Roldan-Valadez E, et al. Right heart catheterization (RHC): A comprehensive review of provocation tests and hepatic hemodynamics in patients with pulmonary hypertension (PH). Curr Probl Cardiol 2022; 47(12): 101351.
[http://dx.doi.org/10.1016/j.cpcardiol.2022.101351] [PMID: 35948196]
[78]
D’Alto M, Dimopoulos K, Coghlan JG, Kovacs G, Rosenkranz S, Naeije R. Right heart catheterization for the diagnosis of pulmonary hypertension. Heart Fail Clin 2018; 14(3): 467-77.
[http://dx.doi.org/10.1016/j.hfc.2018.03.011] [PMID: 29966642]
[79]
Barańska-Pawełczak K, Wojciechowska C, Jacheć W. Diagnostic and predictive value of right heart catheterization-derived measurements in pulmonary hypertension. Wiad Lek 2021; 74(3 cz 1): 546-3.
[http://dx.doi.org/10.36740/WLek202103130]
[80]
Chung K, Strange G, Codde J, Celermajer D, Scalia GM, Playford D. Left heart disease and pulmonary hypertension: Are we seeing the full picture? Heart Lung Circ 2018; 27(3): 301-9.
[http://dx.doi.org/10.1016/j.hlc.2017.09.015] [PMID: 29102471]
[81]
Skoro-Sajer N, Marta G, Gerges C, et al. Surgical specimens, haemodynamics and long-term outcomes after pulmonary endarterectomy. Thorax 2014; 69(2): 116-22.
[http://dx.doi.org/10.1136/thoraxjnl-2013-203746] [PMID: 24052543]
[82]
Kylhammar D, Kjellström B, Hjalmarsson C, et al. A comprehensive risk stratification at early follow-up determines prognosis in pulmonary arterial hypertension. Eur Heart J 2018; 39(47): 4175-81.
[http://dx.doi.org/10.1093/eurheartj/ehx257] [PMID: 28575277]
[83]
Souza R, Jardim C, Julio Cesar Fernandes C, Silveira Lapa M, Rabelo R, Humbert M. NT-proBNP as a tool to stratify disease severity in pulmonary arterial hypertension. Respir Med 2007; 101(1): 69-75.
[http://dx.doi.org/10.1016/j.rmed.2006.04.014] [PMID: 16781131]
[84]
Torres G, Yang J, Griffiths M, et al. Insulin-like growth factor binding Protein-4: A novel indicator of pulmonary arterial hypertension severity and survival. Pulm Circ 2023; 13(2): e12235.
[http://dx.doi.org/10.1002/pul2.12235] [PMID: 37152104]

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