Clinical, laboratory and instrumental evaluation of structural and functional changes of the liver in patients with heart failure

Cover Page

Cite item

Full Text

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


Heart failure is detected in 2% of the population. The leading causes of heart failure are coronary heart disease, arterial hypertension, and valvular heart disease. The number of patients with chronic heart failure continues to increase despite the new methods of diagnosis and treatment. A special contribution is made by damage to target organs in the development of cardiovascular pathology. Impaired liver function or congestive liver is common in heart failure and increases the risk of death and requires further study. The mechanism of liver damage in chronic heart failure is complex and multicomponent. The sensitivity and specificity of standard clinical, laboratory and instrumental methods for the diagnosis of congestive liver are insufficient. With the increase, severity and duration of venous congestion, structural changes in the architectonics occur, leading to the formation of liver fibrosis. The development of cardiac liver fibrosis leads to a complication of the course of chronic heart failure and an increase in mortality.

Among the new diagnostic methods, the most important are serological markers of liver fibrosis, which have high diagnostic accuracy, as well as histological determination of fibrosis, as well as ultrasound examination of the liver in B-mode and determination of liver stiffness by elastography. Direct and indirect serological markers have a higher diagnostic value when using their combination in the composition of panels in the development of hepatopathy of different origins. An increase in the concentration of markers of fibrosis and liver stiffness during elastography correlates with the severity of heart failure and a long-term prognosis for mortality, including from extrahepatic diseases. Performing liver elastography in dynamics allows to monitor the course and treatment of heart failure. The optimal diagnostic method is a combination of direct and indirect markers of fibrosis, ultrasound diagnostics and elastography, in addition to clinical assessment of signs and direct assessment of hemodynamic parameters.

Full Text

Restricted Access

About the authors

Kseniya A. Kisliuk

Saint Petersburg State University; Saint Petersburg City Hospital No. 40 of Kurortny District

Author for correspondence.
ORCID iD: 0000-0003-3828-6692
SPIN-code: 1894-8433

PhD student

Russian Federation, 7-9 Universitetskaya Embankment, Saint Petersburg, 199034; Sestroretsk

Aleksandr N. Bogdanov

Saint Petersburg State University; Saint Petersburg City Hospital No. 40 of Kurortny District

ORCID iD: 0000-0003-1964-3690
Scopus Author ID: 7201674748
ResearcherId: M-5163-2015

MD, Dr. Sci. (Med.), Professor

Russian Federation, 7-9 Universitetskaya Embankment, Saint Petersburg, 199034; Sestroretsk

Sergey G. Shcherbak

Saint Petersburg State University; Saint Petersburg City Hospital No. 40 of Kurortny District

ORCID iD: 0000-0001-5047-2792
SPIN-code: 1537-9822
Scopus Author ID: 485658

MD, Dr. Sci. (Med.), Professor

Russian Federation, 7-9 Universitetskaya Embankment, Saint Petersburg, 199034; Sestroretsk

Svetlana V. Apalko

Saint Petersburg City Hospital No. 40 of Kurortny District

ORCID iD: 0000-0002-3853-4185
SPIN-code: 7053-2507

MD, Cand. Sci. (Biol.)

Russian Federation, Sestroretsk


  1. Metra M, Teerlink JR. Heart Failure. Lancet. 2017;390(10106):1981–1995. doi: 10.1016/s0140-6736(17)31071-1
  2. Ponikowski P, Voors AA, Anker SD, et al. ESC guidelines for the diagnosis and treatment of acute and chronic heart failure: the task force for the diagnosis and treatmtnt of acute and chronic heart failure of the European Society of Cardiology (ESC). Developed with special contribution of the heart failure assotiation (HFA) of the ESC. Eur J Heart Fail. 2016;37(27):2129–2200. doi: 10.1093/eurheartj/ehw128
  3. Fomin IV. Chronic heart failure in russian federation: what do we know and what to do. Russian Journal of Cardiology. 2016;21(8):7–13. (In Russ.). doi: 10.15829/1560-4071-2016-8-7-13
  4. Ketsum ES, Levy WC. Establising prognosing in heart failure: a multimarker approach. Prog Cardiovasc Dis. 2011;54(2):86–96. doi: 10.1016/j.pcad.2011.03.003
  5. Fortea JI, Puente A, Cuadrado A, et al. Cardiac Hepatopathy. Intech Open. 2019. doi: 10.5772/intechopen.89177
  6. Sherlock S. The liver in heart failure: relation of anatomical, functional, and circulatory changes. Br Heart J. 1951;13(3):273–293. doi: 10.1136/hrt.13.3.273
  7. Shah SC, Sass DA. “Cardiac hepatopathy”: a review of liver dysfunction in heart failure. Liver Res Open J. 2015;1(1):1–10. doi: 10.17140/lroj-1-101
  8. Van Deursen VM, Damman K, Hillege HL, et al. Abnormal liver function in relation to hemodynamic profile in heart failure patients. J Card Fail. 2010;16(1):84–90. doi: 10.1016/j.cardfail.2009.08.002
  9. Moller S, Bernardi M. Interaction of the heart and the liver. Eur Heart J. 2013;34(36):2804–2811. doi: 10.1093/eurheartj/eht246
  10. Xanthopoulos A, Starling RC, Kitai T, Triposkiadis F. Heart failure and liver disease: cardiohepatic interactions. JACC Heart Fail. 2019;7(2):87–97. doi: 10.1016/j.jchf.2018.10.007
  11. Yoshihisa A, Sato Y, Yokokawa T, et al. Liver fibrosis score predicts mortality in heart failure patients with preserved ejection fraction. ESC Heart Fail. 2018;5(2):262–270. doi: 10.1002/ehf2.12222
  12. Hisler M, Sanchez W. Congestive hepatopathy. Clin Liver Dis (Hoboken). 2016;8(3):68–71. doi: 10.1002/cld.573
  13. Koehne de Gonzarez AK, Lewkowitch JH. Heart diseases and the liver: pathologic evaluation. Gastroenterol Clin North Am. 2017;46(2):421–435. doi: 10.1016/j.gtc.2017.01.012
  14. Kavoliuniene A, Vaitiekiene A, Cesnaite G. Congestive hepatopathy and hypoxic hepatitis in heart failure: a cardiologist point of view. Int J Cardiol. 2013;166(3):554–558. doi: 10.1016/j.ijcard.2012.05.003
  15. Myers RP, Cerini R, Sayegh R, et al. Cardiac hepatopathy: clinical, hemodynamic, and histologic characteristics and correlation. Hepatology. 2003;37(2):393–400. doi: 10.1053/jhep.2003.50062
  16. Farias AQ, Silvestre OM, Garsia-Tsao G, et al. Serum B-type natriuretic peptide in the initial workup of patients with new onset ascitis: a diagnostic accuracy study. Hepatology. 2014;59(3):1043–1051. doi: 10.1002/hep.26643
  17. Lemmer A, Van-Wagner L, Ganger D. Assessment of advanced liver fibrosis and the risk for hepatic decompensation in patients with congestive hepatopathy. Hepatology. 2018;68(4):1633–1641. doi: 10.1002/hep.30048
  18. Denis C, De Kerguennec C, Bernuau J, et al. Acute hypoxic hepatitis (‘liver shock’): still a frequently overlooked cardiological diagnosis. Eur J Heart Fail. 2004;6(5):561–565. doi: 10.1016/j.ejheart.2003.12.008
  19. Poelzl G, Ess M, Mussner-Seeber C, et al. Liver dysfunction in chronic heart failure: prevalence, characteristics and prognostic significance. Eur J Clin Investig. 2012;42(2):153–163. doi: 10.1111/j.1365-2362.2011.02573.x
  20. Ess M, Mussner-Seeber C, Mariacher S, et al. G-glutamyltransferase rather than total bilirubin predicts outcome in chronic heart failure. J Card Fail. 2011;17(7):577–584. doi: 10.1016/j.cardfail.2011.02.012
  21. Poelzl G, Eberl C, Achrainer H, et al. Prevalence and prognostic significance of elevated-glutamyltransferase in chronic heart failure. Circ. Heart Fail. 2009;2(4):294–302. doi: 10.1161/circheartfailure.108.826735
  22. Shinagava H, Inomata T, Koitabashi T, et al. Increased serum bilirubin levels coincident with heart failure decompensation indicate the need for intravenous inotropic agents. Int Heart J. 2007;48(2):195–204. doi: 10.1536/ihj.48.195
  23. Bradley E, Hendrickson B, Daniels C. Fontan liver disease: review of an emerging epidemic and management options. Curr Treat Options Cardiovasc Med. 2015;17(11):51. doi: 10.1007/s11936-015-0412-z
  24. Wu FM, Kogon B, Earing MG, et al. Liver health in adults with Fontan circulation: A multicenter cross-sectional study. J Thorac Cardiovasc Surg. 2017;153(3):656–664. doi: 10.1016/j.jtcvs.2016.10.060
  25. Amin A, Vakilian F, Maleki M. Serum uric acid levels correlate with filling pressures in systolic heart failure. Congest Heart Fail. 2011;17(2):80–84. doi: 10.1111/j.1751-7133.2010.00205.x
  26. Wells ML, Venkatech SK. Congestive hepatopathy. Abdom Radiol (NY). 2018;43(8):2031–2051. doi: 10.1007/s00261-017-1387-x
  27. Abraldes JG, Sarlieve P, Tandon P. Measurement of portal pressure. Clin Liver Dis. 2014;18(4):779–792. doi: 10.1016/j.cld.2014.07.002
  28. Dhall D, Kim SA, Mc Phaul C, et al. Heterogeneity of fibrosis in liver biopsies of patients with heart failure undergoing heart transplant evaluation. Am J Surg Pathol. 2018;42(12):1617–1624. doi: 10.1097/pas.0000000000001163
  29. Samsky MD, Patel CB, DeWald TA, et al. Cardiohepatic interaction in heart failure: an overwiew and clinical implications. J Am Coll Cardiol. 2013;61(24):2397–2405. doi: 10.1016/j.jacc.2013.03.042
  30. Bosch DE, Koro K, Richards E, et al. Validation of a congestive hepatic fibrosis score system. Am J Surg Pathol. 2019;43(6):766–772. doi: 10.1097/pas.0000000000001250
  31. Chin JL, Pavlides M, Moolla A, Ryan JD. Non-invasive markers of liver fibrosis: adjuncts or alternatives to liver biopsy? Front Pharmacol. 2016;7:159. doi: 10.3389/fphar.2016.00159
  32. Veidal SS, Bay-Jensen AC, Tougas G, et al. Serum markers of liver fibrosis: combining the BIPED classification and the neo-epitope approach in the development of new biomarkers. Dis Markers. 2010;28(1):15–28. doi: 10.3233/DMA-2010-0678
  33. Henderson NC, Arnold TD, Katamura Y, et al. Targeting of av integrin identifies a core molecular pathway that regulates fibrosis in several organs. Nat. Med. 2013;19(12):1617–1624. doi: 10.1038/nm.3282
  34. Gressner OA, Weiskirchen R, Gressner AM. Biomarkers of liver fibrosis: clinical translation of molecular pathogenesis or based on liver-dependent malfunction tests. Clin Chim Acta. 2007;381(12):107–113. doi: 10.1016/j.cca.2007.02.038
  35. EASL-ALEH Clinical Practice Guidelines: Non-invasive tests for evaluation of liver disease severity and prognosis. J Hepatol. 2015;63(1):237–264. doi: 10.1016/j.jhep.2015.04.006
  36. Boursier J, Vergniol J, Guillet A, et al. Diagnostic accuracy and prognostic significance of blood fibrosis tests and liver stiffness measurement by FibroScan in non-alcoholicfatty liver disease. J Hepatol. 2016;65(3):570–578. doi: 10.1016/j.jhep.2016.04.023
  37. Genkel’ VV, Hasanova RO, Koljadich MI. Determinants of increased serum markers of liver fibrosis in patients with chronic heart failure. Experimental and Clinical Gastroenterology Journal. 2019;(6(166)):37–43. (In Russ.). doi: 10.31146/1682-8658-ecg-166-6-37-43
  38. Stolbova SK, Dragomiretskaya NА, Beliaev IG, Podzolkov VI. Clinical and laboratory associations of liver fibrosis indexes in patients with decompensated chronic heart failure II-IV functional classes. Kardiologiia. 2020;60(5):90–99. (In Russ.). doi: 10.18087/cardio.2020.5.n920
  39. Patel K, Sebastiani G. Limitations of non-invasive tests for assessment of liver fibrosis. JHEP Rep. 2020;2(2):100067. doi: 10.1016/j.jhepr.2020.100067
  40. Ozturk A, Grajo JR, Dhyani M, et al. Principles of ultrasound elastography. Abdom Radiol (NY). 2018;43(4):773–785. doi: 10.1007/s00261-018-1475-6
  41. Shiina T, Nightingale KR, Palmeri ML, et al. WFUMB guidelines and recommendations for clinical use of ultrasound elastography: part 1: basic principles and terminology. Ultrasound Med Biol. 2015;41(5):1126–1147. doi: 10.1016/j.ultrasmedbio.2015.03.009
  42. Babu AS, Wells ML, Teytelboym OM, et al. Elastography in chronic liver disease: modalities, techniques, limitations and future directions. Radiographics. 2016;36(7):1987–2006. doi: 10.1148/rg.2016160042
  43. Ferraioli G, Barr RG. Ultrasound liver elastography beyond liver fibrosis assessment. World J Gastroenterol. 2020;26(24):3413–3420. doi: 10.3748/wjg.v26.i24.3413
  44. Lebray P, Varnous S, Charlotte F, et al. Liver stiffness is an unreliable marker of liver fibrosis in patients with cardiac insufficiency. Hepatology. 2008;48(6):2089. doi: 10.1002/hep.22594
  45. Millonig G, Friedrich S, Adolf S, et al. Liver stiffness is directly influenced by central venous pressure. J Hepatol. 2010;52(2):206–210. doi: 10.1016/j.jhep.2009.11.018
  46. Taniguchi T, Sakata Y, Ohtani T, et al. Usefulness of transient elastography for noninvasive and reliable estimation of right-sided filling pressure in heart failure. Am J Cardiol. 2014;113(3):552–558. doi: 10.1016/j.amjcard.2013.10.018
  47. Taniguchi T, Ohtani T, Kioka H, et al. Liver stiffness reflecting right-sided filling pressure can predict adverse outcomes in patients with heart failure. JACC Cardiovasc Imaging. 2019;12(6):955–964. doi: 10.1016/j.jcmg.2017.10.022
  48. Omote K, Nagai T, Asakawa N, et al. Impact of admission liver stiffness on long-term clinical outcomes in patients with acute decompensated heart failure. Heart Vessels. 2019;34(6):984–991. doi: 10.1007/s00380-018-1318-y
  49. Saito Y, Kato M, Nagashima K, et al. Prognostic relevance of liver stiffness assessed by transient elastography in patients with acute decompensated heart failure. Circ J. 2018;82(7):1822–1829. doi: 10.1253/circj.cj-17-1344
  50. Colli A, Pozzoni P, Berzuini A, et al. Decompensated chronic heart failure: Increased liver stiffness measured by means of transient elastography. Radiology. 2010;257(3):872–878. doi: 10.1148/radiol.10100013
  51. Alegre F, Herrero JI, Iñarrairaegui M, et al. Increased liver stiffness values in patients with heart failure. Acta Gastroenterol Belg. 2013;76(2):246–250.
  52. Solov’eva AE, Kobalava ZhD, Villeval’de SV, et al. Prognostic value of liver stiffness in decompensated heart failure: results of prospective observational transient elastography-based study. Kardiologija. 2018;58(S10):20–32. (In Russ.). doi: 10.18087/cardio.2488
  53. Potthoff A, Schettler A, Attia D, et al. Liver stiffness measurements and short-term survival after left ventricular assist device implantation: A pilot study. J Heart Lung Transplant. 2015;34(12):1586–1594. doi: 10.1016/j.healun.2015.05.022
  54. Nishi H, Toda K, Miyagawa S, et al. Novel method of evaluating liver stiffness using transient elastography to evaluate perioperative status in severe heart failure. Circ J. 2015;79(2):391–397. doi: 10.1253/circj.cj-14-0929
  55. Fang C, Konstantatou E, Romanos O, et al. Reproducibility of 2-dimensional shear wave elastography assessment of the liver: a direct comparison with point shear wave elastography in healthy volunteers. J Ultrasound Med. 2017;36(8):1563–1569. doi: 10.7863/ultra.16.07018
  56. Avila DX, Matos PA, Quintino G, et al. Diagnostic and prognostic role of liver elastography in heart failure. Int J Cardiovasc Sci. 2019;33(3):227–232. doi: 10.36660/ijcs.20190005
  57. Balashova AA, Arisheva OS, Garmash IV, et al. Diagnosis of liver fibrosis in patients with heart failure. Klinicheskaja farmakologija i terapija. 2017;26(3):7–12. (In Russ.)

Supplementary files

There are no supplementary files to display.

Copyright (c) 2021 Kisliuk K.A., Bogdanov A.N., Shcherbak S.G., Apalko S.V.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.

СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 71733 от 08.12.2017.

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies