Role of surfactant proteins in development of pulmonary edema

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

INTRODUCTION: The problem of pulmonary edema is relevant in the modern world, since despite significant progress in understanding the etiology, pathogenesis and approaches to treatment, mortality reaches 50%. The complexity and relevance of the problem are associated with differential diagnosis of cardiogenic and non-cardiogenic pulmonary edema, which is of principal significance in selection of treatment and diagnostic tactic.

AIM: Based on the literature data, to analyze the diagnostic role of surfactant protein (SP) as a biomarker of pulmonary edema.

Traditional analysis of cardiogenic pulmonary edema implies the development of high pressure in the pulmonary capillaries, which creates hydrostatic gradients for the flow of fluid from capillaries into the interstitial and alveolar spaces. Experimental studies were conducted on animals with modeled pulmonary edema, clinical studies of the pulmonary barrier dysfunction were conducted in patients with pulmonary edema. Studies on animal models show that high pressure in capillaries can cause disruption of the barrier in alveolar-capillary cells, which increases permeability and transport of fluid and protein into the lung parenchyma, with the subsequent dysfunction of surfactant. As reported in literature, some patients with cardiogenic pulmonary edema have elevated plasma levels of SP and tumor necrosis factor alpha, which reflects disruption of the barrier and acute tissue injury, respectively. Studies conducted in patients with chronic heart failure and impaired gas exchange have determined increase in the number of alveolar type II cells and increase in SP level in plasma.

CONCLUSION: Thus, the conducted studies suggest that acute rise of capillary pressure can cause lung injury, destruct the barrier, and contribute to the overproduction of fluid both through hydrostatic mechanisms, and through alteration of the permeability of alveolar–capillary barrier. Upon that, patients with cardiogenic pulmonary edema had high SP levels in plasma.

Full Text

Restricted Access

About the authors

Liya R. Pakhnova

Astrakhan State Medical University

Author for correspondence.
Email: pahnova@mail.ru
ORCID iD: 0000-0002-4021-325X
SPIN-code: 3631-1791
Scopus Author ID: 57209748537

MD, Cand. Sci. (Med.)

Russian Federation, Astrakhan

Lyudmila P. Voronina

Astrakhan State Medical University

Email: voroninaluda74@mail.ru
ORCID iD: 0000-0002-2395-745X
SPIN-code: 4472-1574

Cand. Sci (Med.), Associate Professor

Russian Federation, Astrakhan

Dmitry V. Pakhnov

Astrakhan State Medical University

Email: pahnov1@mail.ru
ORCID iD: 0000-0002-7803-8661
SPIN-code: 8269-5808

Cand. Sci (Med.), Associate Professor

Russian Federation, Astrakhan

References

  1. Komiya K, Akaba T, Kozaki Y, et al. A systematic review of diagnostic methods to differentiate acute lung injury/acute respiratory distress syndrome from cardiogenic pulmonary edema. Crit Care. 2017;21(1):228. doi: 10.1186/s13054-017-1809-8
  2. Tereshchenko SN, Zhirov IV, Nasonova SN, et al. Pathophysiology of acute heart failure. What’s new? Russ J Cardiol. 2016;(9):52–64. (In Russ). doi: 10.15829/1560-4071-2016-9-52-64
  3. Mareev VYu, Fomin IV, Ageev FT, et al.; Russian Heart Failure Society, Russian Society of Cardiology. Russian Scientific Medical Society of Internal Medicine Guidelines for Heart failure: chronic (CHF) and acute decompensated (ADHF). Diagnosis, prevention and treatment. Kardiologiia. 2018;58(6S):8–158. (In Russ). doi: 10.18087/cardio.2475
  4. Wright JR. Immunoregulatory functions of surfactant proteins. Nat Rev Immunol. 2005;5(1):58–68. doi: 10.1038/nri1528
  5. Casals C. Role of surfactant protein A (SP-A)/lipid interactions for SP-A functions in the lung. Pediatr Pathol Mol Med. 2001;20(4): 249–68. doi: 10.1080/15513810109168821
  6. Vieira F, Kung JW, Bhatti F. Structure, genetics and function of the pulmonary associated surfactant proteins A and D: The extra-pulmonary role of these C type lectins. Ann Anat. 2017;211:184–201. doi: 10.1016/j.aanat.2017.03.002
  7. Arroyo R, Echaide M, Moreno–Herrero F, et al. Functional characterization of the different oligomeric forms of human surfactant protein SP-D. Biochim Biophys Acta Proteins Proteom. 2020;1868(8):140436. doi: 10.1016/j.bbapap.2020.140436
  8. Okazaki S, Murai H, Kidoguchi S, et al. The Biomarker Salivary SP-D may Indicate Small Airway Inflammation and Asthma Exacerbation. J Investig Allergol Clin Immunol. 2017;27(5):305–12. doi: 10.18176/jiaci.0174
  9. Dy ABC, Arif MZ, Addison KJ, et al. Genetic Variation in Surfactant Protein-A2 Delays Resolution of Eosinophilia in Asthma. J Immunol. 2019;203(5):1122–30. doi: 10.4049/jimmunol.1900546
  10. Yoshikawa T, Otsuka M, Chiba H, et al. Surfactant protein A as a biomarker of outcomes of anti-fibrotic drug therapy in patients with idiopathic pulmonary fibrosis. BMC Pulm Med. 2020;20(1):27. doi: 10.1186/s12890-020-1060-y
  11. Reynolds P, Bustani P, Darby C, et al. Less-Invasive Surfactant Administration for Neonatal Respiratory Distress Syndrome: A Consensus Guideline. Neonatology. 2021;118(5):586–92. doi: 10.1159/000518396
  12. Schicke E, Cseresnyés Z, Rennert K, et al. Staphylococcus aureus Lung Infection Results in Down-Regulation of Surfactant Protein-A Mainly Caused by Pro-Inflammatory Macrophages. Microorganisms. 2020;8(4):577. doi: 10.3390/microorganisms8040577
  13. Kendall M, Ding P, Mackay R–M, et al. Surfactant protein D (SP-D) alters cellular uptake of particles and nanoparticles. Nanotoxicology. 2013;7(5):963–73. doi: 10.3109/17435390.2012.689880
  14. Hou X, Zhang X, Zhang Z. Role of surfactant protein-D in ocular bacterial infection. Int Ophthalmol. 2022;42(11):3611–23. doi: 10.1007/s10792-022-02354-x
  15. Posa A, Paulsen F, Dietz R, et al. Quantification of surfactant proteins in tears of patients suffering from dry eye disease compared to healthy subjects. Ann Anat. 2018;216:90–4. doi: 10.1016/j.aanat.2017.11.006
  16. Yang Y, Li Q, Tan F, et al. Mechanism of IL-8-induced acute lung injury through pulmonary surfactant proteins A and B. Exp Ther Med. 2020;19(1):287–93. doi: 10.3892/etm.2019.8192
  17. Lee YS. Electron microscopic studies on the alveolar-capillary barrier in the patients of chronic pulmonary edema. Jpn Circ J. 1979;43(10):945–54. doi: 10.1253/jcj.43.945
  18. West JB. Invited review: pulmonary capillary stress failure. J Appl Physiol (1985). 2000;89(6):2483–9; discussion 2497. doi: 10.1152/jappl.2000.89.6.2483
  19. Pappas L, Filippatos G. Pulmonary congestion in acute heart failure: from hemodynamics to lung injury and barrier dysfunction. Rev Esp Cardiol. 2011;64(9):735–8. (In Spanish). doi: 10.1016/j.recesp.2011.05.006
  20. Tsukimoto K, Mathieu–Costello O, Prediletto R, et al. Ultrastructural appearances of pulmonary capillaries at high transmural pressures. J Appl Physiol (1985). 1991;71(2):573–82. doi: 10.1152/jappl.1991. 71.2.573
  21. Bredenberg CE, Nieman GF, Paskanik AM, et al. Microvascular membrane permeability in high surface tension pulmonary edema. J Appl Physiol (1985). 1986;60(1):253–9. doi: 10.1152/jappl. 1986.60.1.253
  22. Bachofen H, Schürch S, Michel RP, et al. Experimental hydrostatic pulmonary edema in rabbit lungs. Morphology. Am Rev Respir Dis. 1993;147(4):989–96. doi: 10.1164/ajrccm/147.4.989
  23. West JB, Mathieu–Costello O, Jones JH, et al. Stress failure of pulmonary capillaries in racehorses with exercise–induced pulmonary hemorrhage. J Appl Physiol (1985). 1993;75(3):1097–109. doi: 10.1152/jappl.1993.75.3.1097
  24. Tomonaga T, Izumi H, Yoshiura Y, et al. Examination of Surfactant Protein D as a Biomarker for Evaluating Pulmonary Toxicity of Nanomaterials in Rat. Int J Mol Sci. 2021;22(9):4635. doi: 10.3390/ijms22094635
  25. Haworth SG, Hall SM, Patel M, et al. Peripheral pulmonary vascular and airway abnormalities in adolescents with rheumatic mitral stenosis. Int J Cardiol. 1988;18(3):405–16. doi: 10.1016/0167-5273(88)90059-9
  26. Doyle IR, Nicholas TE, Bersten AD. Serum surfactant protein-A levels in patients with acute cardiogenic pulmonary edema and adult respiratory distress syndrome. Am J Respir Crit Care Med. 1995;152(1):307–17. doi: 10.1164/ajrccm.152.1.7599839
  27. Shimura S, Masuda T, Takishima T, et al. Surfactant apoprotein-A concentration in airway secretions for the detection of pulmonary oedema. Eur Respir J. 1996;9(12):2525–30. doi: 10.1183/09031936.96.09122525
  28. Günther A, Siebert C, Schmidt R, et al. Surfactant alterations in severe pneumonia, acute respiratory distress syndrome, and cardiogenic lung edema. Am J Respir Crit Care Med. 1996;153(1): 176–84. doi: 10.1164/ajrccm.153.1.8542113
  29. De Pasquale CG, Arnolda LF, Doyle IR, et al. Plasma surfactant protein-B: a novel biomarker in chronic heart failure. Circulation. 2004;110(9):1091–6. doi: 10.1161/01.cir.0000140260.73611.fa
  30. De Pasquale CG, Arnolda LF, Doyle IR, et al. Circulating surfactant protein-B levels increase acutely in response to exercise–induced left ventricular dysfunction. Clin Exp Pharmacol Physiol. 2005;32(8): 622–7. doi: 10.1111/j.0305-1870.2005.04241.x
  31. Magrì D, Brioschi M, Banfi C, et al. Circulating plasma surfactant protein type B as biological marker of alveolar-capillary barrier damage in chronic heart failure. Circ Heart Fail. 2009;2(3):175–80. doi: 10.1161/circheartfailure.108.819607
  32. Magrì D, Banfi C, Maruotti A, et al. Plasma immature form of surfactant protein type B correlates with prognosis in patients with chronic heart failure. A pilot single-center prospective study. Int J Cardiol. 2015;201:394–9. doi: 10.1016/j.ijcard.2015.08.105
  33. Lüers C, Hagenah G, Wachter R, et al. Importance of surfactant proteins B and D for the differential diagnosis of acute dyspnea. Med Klin (Munich). 2010;105(9):611–8. (In German). doi: 10.1007/s00063-010-1100-0
  34. Agostoni P, Banfi C, Magrì D, et al. Kinetics of plasma SPB and RAGE during mechanical ventilation in patients undergoing major vascular surgery. Respir Physiol Neurobiol. 2011;178(2):256–60. doi: 10.1016/j.resp.2011.06.019
  35. Hill J, Heslop C, Man SFP, et al. Circulating surfactant protein-D and the risk of cardiovascular morbidity and mortality. Eur Heart J. 2011;32(15):1918–25. doi: 10.1093/eurheartj/ehr124
  36. Gargiulo P, Banfi C, Ghilardi S, et al. Surfactant-Derived Proteins as Markers of Alveolar Membrane Damage in Heart Failure. PLoS One. 2014;9(12):e115030. doi: 10.1371/journal.pone.0115030
  37. Brankovic M, Akkerhuis KM, Mouthaan H, et al. Utility of temporal profiles of new cardio-renal and pulmonary candidate biomarkers in chronic heart failure. Int J Cardiol. 2019;276:157–65. doi: 10.1016/j.ijcard.2018.08.001
  38. Banfi C, Brioschi M, Karjalainen MK, et al. Immature surfactant protein-B impairs the antioxidant capacity of HDL. Int J Cardiol. 2019;285:53–8. doi: 10.1016/j.ijcard.2019.02.057
  39. Banfi C, Gugliandolo P, Paolillo S, et al. The alveolar-capillary unit in the physiopathological conditions of heart failure: identification of a potential marker. Eur J Prev Cardiol. 2023;30(Suppl 2):ii2–8. doi: 10.1093/eurjpc/zwad227
  40. Zanza C, Saglietti F, Tesauro M, et al. Cardiogenic Pulmonary Edema in Emergency Medicine. Adv Respir Med. 2023;91(5):445–63. doi: 10.3390/arm91050034

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2025 Eco-Vector


Media Registry Entry of the Federal Service for Supervision of Communications, Information Technology and Mass Communications (Roskomnadzor) PI No. FS77-76803 dated September 24, 2019.