Hepatopulmonary syndrome and liver transplantation: the review and a case report
https://doi.org/10.23873/2074-0506-2017-9-1-23-34
Abstract
Hepatopulmonary syndrome is a liver disease complication characterized by the clinical triad of an advanced chronic liver disease, a pulmonary vascular dilatation, and a reduced arterial oxygenation (hypoxemia: PaO2 less than 70 mm Hg at rest) in the absence of intrinsic cardiopulmonary disease. Precapillary vasodilatation, intrapulmonary angiogenesis and hyperdynamic circulation lead to arteriovenous shunting and reduced gas diffusion. In case of detecting macroscopic shunts, the pulmonary artery branch embolization could be performed. However, the hepatopulmonary syndrome can be cured nowadays by means of liver transplantation only. A 5-year survival in these patients is about 70%. The observed mortality is the highest during the surgery or early after, especially in patients with PaO2 lower than 50 mm Hg. It ranges from 8.5 to 29%. A prolonged oxygenation support is often required after liver transplantation using invasive or non-invasive ventilation, or even extracorporeal membrane oxygenation. In this review, we have focused on the recent advances in this field as described in available literature and have presented a case report of successful liver transplantation in a patient with a severe hepatopulmonary syndrome.
About the Authors
Yu. O. Malinovskaya
Moscow Regional Research and Clinical Institute n.a. M.F. Vladimirskiy
Russian Federation
Russian Federation
Research Fellow of the Abdominal Surgery Unit
Moscow, Russia
D. Dzhiner
I.M. Sechenov First Moscow State Medical University
Russian Federation
Moscow, Russia
Russian Federation
Moscow, Russia
E. N. Ostroumov
N.V. Sklifosovsky Research Institute for Emergency Medicine
Russian Federation
Moscow, Russia
Russian Federation
Moscow, Russia
Ya. G. Moysyuk
Moscow Regional Research and Clinical Institute n.a. M.F. Vladimirskiy
Russian Federation
Moscow, Russia
Russian Federation
Moscow, Russia
References
1. Aldenkortt F., Aldenkortt M., Caviezel L., et al. Portopulmonary hypertension and hepatopulmonary syndrome. World J Gastroenterol. 2014;20(25):8072–8081. PMID:25009379 DOI:10.3748/wjg.v20.i25.8072
2. Zhang Z., et al. Hepatopulmonary syndrome: the role of intra-abdominal hypertension and a novel mouse model. Int J Clin Exp Pathol. 2014;7(2):768–773. PMID:24551301
3. Tumgor G. Cirrhosis and hepatopulmonary syndrome. World J Gastroenterol. 2014;20(10):2586–2594. PMID:24627594 DOI:10.3748/wjg.v20.i10.2586
4. Tzovaras N., Stefos A., Georgiadou S.P., et al. Reversion of severe hepatopulmonary syndrome in a non cirrhotic patient after corticosteroid treatment for granulomatous hepatitis: a case report and review of the literature. World J Gastroenterol. 2006;12(2):336–339. PMID:16482641
5. Gupta D., Vijaya D.R., Gupta R., et al. Prevalence of hepatopulmonary syndrome in cirrhosis and extrahepatic portal venous obstruction. Am J Gastroenterol. 2001;96(12):3395–3399. PMID:11774955 DOI:10.1111/j.1572-0241.2001.05274.x
6. Sari S., Oguz D., Sucak T., et al. He patopulmonary syndrome in children with cirrhotic and non-cirrhotic portal hypertension: a single-center experience. Dig Dis Sci. 2012;57(1):175–1781. PMID:21792618 DOI:10.1007/s10620-011-1832-6
7. De B.K., Sen S., Biswas P.K., et al. Occurrence of hepatopulmonary syndrome in Budd-Chiari syndrome and the role of venous decompression. Gastroenterology. 2002;122(4):897–903. PMID:11910341
8. Ivashkin V.T., Morozova M.A., Maevskaya M.V. Hepatopulmonary syndrome: diagnosis, pathogenesis, clinical symptoms and treatment methods. RZhGGK. 2008;18(1):12–17. (In Russian).
9. Valenti A., Caimi G. Physiopathological, clinical and therapeutic aspects of hepatopulmonary syndrome. Clin Ter. 2010;161(3):e123–128. PMID:20589345
10. Grace J.A., Angus P.W. Hepatopulmonary syndrome: update on recent advances in pathophysiology, investigation, and treatment. J Gastroenterol Hepatol. 2013;28(2): 213–219. PMID:23190201 DOI:10.1111/jgh.12061
11. Machicao V.I., Fallon M.B. Hepatopulmonary syndrome. Semin Respir Crit Care Med. 2012;33(1):11–16. PMID:22447256 DOI:10.1055/s-0032-1301730
12. Enache I., Oswald-Mammosser M., Woehl-Jaegle M.L., et al. Cirrhotic cardiomyopathy and hepatopulmonary syndrome: prevalence and prognosis in a series of patients. Respir Med. 2013;107(7):1030–1036. PMID:23615223 DOI:10.1016/j.rmed.2013.03.010
13. Valley M.A., Trotter J.F., Thomas D., et al. The relationship between hepatopulmonary syndrome and altitude. Can J Gastroenterol Hepatol. 2014;28(3):140– 142. PMID:24619635
14. Gorgy A.I., Jonassaint N.L., Stanley S.E., et al. Hepatopulmonary Syndrome Is a Frequent Cause of Dyspnea in the Short Telomere Disorders. Chest. 2015;148(4):1019– 1026. PMID:26158642 DOI:10.1378/chest.15-0825
15. Roberts K.E., Kawut S.M., Krowka M.J., et al. Genetic risk factors for hepatopulmonary syndrome in patients with advanced liver disease. Gastroenterology. 2010;139(1):130–139.e24. PMID:20346360 DOI:10.1053/j.gastro.2010.03.044
16. Feng G., Rong H. The role of hemodynamic and vasoactive substances on hepatopulmonary syndrome. Eur Rev Med Pharmacol Sci. 2014;18(3):380–386. PMID:24563438
17. Fritz J.S., Fallon M.B., Kawut S.M. Pulmonary vascular complications of liver disease. Am J Respir Crit Care Med. 2013;187(2):133–143. PMID:23155142 DOI:10.1164/rccm.201209-1583CI
18. Khan A.N., Al-Jahdali H., Abdullah K., et al. Pulmonary vascular complications of chronic liver disease: Pathophy siology, imaging, and treatment. Ann Thorac Med. 2011;6(2):57–65. PMID:21572693 DOI:10.4103/1817-1737.78412
19. Rodriguez-RoisinR., Krowka M.J. Hepatopulmonary syndrome--a li verinduced lung vascular disorder. N Engl J Med. 2008;358(22):2378–2387. PMID:18509123 DOI:10.1056/NEJMra0707185
20. Macedo L.G., Lopes E.P. Hepatopulmonary syndrome: an update. Sao Paulo Med J. 2009;127(4):223–230. PMID:20011928
21. Polavarapu N., Tripathi D. Liver in cardiopulmonary disease. Best Pract Res Clin Gastroenterol. 2013;27(4):497– 512. PMID:24090938 DOI:10.1016/j.bpg.2013.06.020
22. Chihara Y., Egawa H., Tsuboi T., et al. Immediate noninvasive ventilation may improve mortality in patients with hepatopulmonary syndrome after liver transplantation. Liver Transpl. 2011;17(2):144–148. PMID:21280187 DOI:10.1002/lt.22207
23. Zhang J., Yang W., Luo B., et al. The role of CX(3)CL1/CX(3)CR1 in pulmonary angiogenesis and intravascular monocyte accumulation in rat experimental hepatopulmonary syndrome. J Hepatol. 2012;57(4):752–758. PMID:22659346 DOI:10.1016/j.jhep.2012.05.014
24. Zhang Z.J., Yang C.Q. Progress in investigating the pathogenesis of hepatopulmonary syndrome. Hepatobiliary Pancreat Dis Int. 2010;9(4):355–360. PMID:20688597
25. Cremona G., Higenbottam T.W., Mayoral V., et al. Elevated exhaled nitric oxide in patients with hepatopulmonary syndrome. Eur Respir J. 1995;8(11):1883–1885. PMID:8620957
26. Guo S.B., Duan Z.J., Li Q., Sun X.Y. Effects of heme oxygenase-1 on pulmonary function and structure in rats with liver cirrhosis. Chin Med J (Engl). 2011;124(6):918–922. PMID:21518603
27. Ali O.M., Agarwal A., Akram S. Platypnea orthodeoxia: a 'laid-back' case of dyspnoea. BMJ Case Rep. 2013;2013. PII:bcr2012007810. PMID:23362060 DOI:10.1136/bcr-2012-007810
28. Fallesen C.O., Sondergaard L., Nissen H. Platypnoea-orthodeoxia: a rare cause of severe dyspnoea. Ugeskr Laeger. 2013;175(47A). PII:V11120636. PMID:25353093
29. Silverio Ade O., Guimarães D.C., Elias L.F., et al. Are the spider angiomas skin markers of hepatopulmonary syndrome? Arq Gastroenterol. 2013;50(3):175–179. PMID:24322187 DOI:10.1590/S0004-28032013000200031
30. Gaber R., Ziada D.H., Kotb N.A., et al. Detection of hepatopulmonary syndrome in patients with liver cirrhosis using 3D contrast echocardiography. Arab J Gastroenterol. 2012;13(1):14– 19. PMID:22560819 DOI:10.1016/j.ajg.2012.03.004.
31. Porres-Aguilar M., Gallegos-Orozco J.F., Garcia H., et al. Pulmonary vascular complications in portal hypertension and liver disease: a concise review. Rev Gastroenterol Mex. 2013;78(1):35–44. PMID:23369639 DOI:10.1016/j.rgmx.2012.10.004.
32. Awad Mel D., El-Arabi H.A., El-Sharnouby K.A., Abo Dewan K.A. Diagnostic evaluation of hepatopulmonary syndrome in Egyptian children with chronic liver disease. J Egypt Soc Parasitol. 2014;44(1):97–112. PMID:24961015
33. Kochar R., Tanikella R., Fallon M.B. Serial pulse oximetry in hepatopulmonary syndrome. Dig Dis Sci. 2011;56(6):1862–1868. PMID:21327708 DOI:10.1007/s10620-011-1600-7
34. Suceveanu A.I., Mazilu L., Tomescu D., et al. Screening of hepatopulmonary syndrome (HPS) with CEUS and pulse-oximetry in liver cirrhosis patients eligible for liver transplant. Chirurgia (Bucur). 2013;108(5):684–688. PMID:24157113
35. Khabbaza J.E., Krasuski R.A., Tonelli A.R. Intrapulmonary shunt confirmed by intracardiac echocardiography in the diagnosis of hepatopulmonary syndrome. Hepatology. 2013;58(4):1514–1515.PMID:23696309 DOI:10.1002/hep.26482
36. Fischer C.H., Campos O., Fernandes W.B., et al. Role of contrast-enhanced transesophageal echocardiography for detection of and scoring intrapulmonary vascular dilatation. Echocardiography. 2010;27(10):1233–1237. PMID:20584052 DOI:10.1111/j.1540-8175.2010.01228.x
37. Porres-Aguilar M., Altamirano J.T., Torre-Delgadillo A., et al. Portopulmonary hypertension and hepatopulmonary syndrome: a clinicianoriented overview. Eur Respir Rev. 2012;21(125):223–233. PMID:22941887 DOI:10.1183/09059180.00007211
38. El-Shabrawi M.H., Omran S., Wageeh S., et al. (99m)Technetium-macroaggregated albumin perfusion lung scan versus contrast enhanced echocardiography in the diagnosis of the hepatopulmonary syndrome in children with chronic liver disease. Eur J. Gastroenterol Hepatol. 2010;22(8):1006–1012. PMID:20101183 DOI:10.1097/MEG.0b013e328336562e
39. Abrams G.A., Jaffe C.C., Hoffer P.B., et al. Diagnostic utility of contrast echocardiography and lung perfusion scan in patients with hepatopulmonary syndrome. Gastroenterology. 1995;109(4):1283–1288. PMID:7557096
40. Saad N.E., Lee D.E., Waldman D.L., Saad W.E. Pulmonary arterial coil embolization for the management of persistent type I hepatopulmonary syndrome after liver transplantation. J Vasc Interv Radiol. 2007;18(12):1576–1580. PMID:18057294 DOI:10.1016/j.jvir.2007.08.008
41. Krowka M.J., Fallon M.B., Kawut S.M., et al. International Liver Transplant Society Practice Guidelines: Diagnosis and Management of Hepatopulmonary Syndrome and Portopulmonary Hypertension. Transplantation. 2016;100(7):1440–1452. PMID:27326810 DOI:10.1097/TP.0000000000001229
42. Gupta S., Faughnan M.E., Lilly L., et al. Norfloxacin therapy for hepatopulmonary syndrome: a pilot randomized controlled trial. Clin Gastroenterol Hepatol. 2010;8(12):1095–1098. PMID:20816858 DOI:10.1016/j.cgh.2010.08.011
43. Kianifar H.R., Khalesi M., Mahmoodi E., Afzal Aghaei M. Pentoxifylline in hepatopulmonary syndrome. World J Gastroenterol. 2012;18(35):4912–4916. PMID:23002364 DOI:10.3748/wjg.v18.i35.4912
44. Roma J., Balbi E., Pacheco-Moreira L., et al. Methylene blue used as a bridge to liver transplantation postoperative recovery: a case report. Transplant Proc. 2010;42(2):601–604. PMID:20304203 DOI:10.1016/j.transproceed.2010.01.003
45. Chang C.C., Wang S.S., Hsieh H.G., et al. Rosuvastatin improves hepatopulmonary syndrome through inhibition of inflammatory angiogenesis of lung. Clin Sci (Lond). 2015;129(6):449–460. PMID:25940601 DOI:10.1042/CS20140622
46. Zhao Z., Liu L., Liu N., et al. The therapeutic effects of tumor necrosis factoralpha monoclonal antibody on hepatopulmonary syndrome in rats. Xi Bao Yu Fen Zi Mian Yi Xue Za Zhi. 2010;26(7):657–659;662. PMID:20619089
47. Huang X., Liu L.I., Liu N. Molecular mechanism of tumor necrosis factoralpha monoclonal antibody in hepatopulmonary syndrome in rats. Zhonghua Gan Zang Bing Za Zhi. 2015;23(6):458–463. PMID:26236934 DOI:10.3760/cma.j.issn.1007-3418.2015.06.013
48. Wallace M.C., James A.L., Marshall M., Kontorinis N. Resolution of severe hepatopulmonary syndrome following transjugular portosystemic shunt procedure. BMJ Case Rep. 2012;2012. PII:bcr0220125811. PMID:22669921 DOI:10.1136/bcr.02.2012.5811
49. Martinez-Palli G., Drake B.B., Garcia-Pagan J.C., et al. Effect of transjugular intrahepatic portosystemic shunt on pulmonary gas exchange in patients with portal hypertension and hepatopulmonary syndrome. World J Gastroenterol. 2005;11(43):6858– 6862. PMID:16425397
50. Tsauo J., Weng N., Ma H., et al. Role of Transjugular Intrahepatic Portosystemic Shunts in the Management of He patopulmonary Syndrome: A Systemic Literature Review. J Vasc Interv Radiol. 2015;26(9):1266–1271. PMID:26074026 DOI:10.1016/j.jvir.2015.04.017
51. Lee H.W., Suh K.S., Kim J., et al. Pulmonary artery embolotherapy in a patient with type I hepatopulmonary syndrome after liver transplantation. Korean J Radiol. 2010;11(4):485–489. PMID:20592935 DOI:10.3348/kjr.2010.11.4.485
52. Grady K., Gowda S., Kingah P., Soubani A.O. Coil embolization of pulmonary arteries as a palliative treatment of diffuse type I hepatopulmonary syndrome. Respir Care. 2015;60(2):e20–25. PMID:25185147 DOI:10.4187/respcare.03198.
53. Nayyar D., Man H.S., Granton J., Gupta S. Defining and characterizing severe hypoxemia after liver transplantation in hepatopulmonary syndrome. Liver Transpl. 2014;20(2):182–190. PMID:24142412 DOI:10.1002/lt.23776
54. Goldberg D.S., Krok K., Batra S., et al. Impact of the hepatopulmonary syndrome MELD exception policy on outcomes of patients after liver transplantation: an analysis of the UNOS database. Gastroenterology. 2014;146(5):1256–1265.e1. PMID:24412528 DOI:10.1053/j.gastro.2014.01.005
55. EASL Clinical Practice Guidelines: Liver transplantation. J Hepatol. 2016;64(2):433–485. PMID:26597456 DOI:10.1016/j.jhep.2015.10.006.
56. Pascasio J.M., Grilo I., López-Pardo F.J., et al. Prevalence and severity of hepatopulmonary syndrome and its influence on survival in cirrhotic patients evaluated for liver transplantation. Am J Transplant. 2014;14(6):1391–1399. PMID:24730359 DOI:10.1111/ajt.12713
57. Iyer V.N., Swanson K.L., Cartin-Ceba R., et al. Hepatopulmonary syndrome: favorable outcomes in the MELD exception era. Hepatology. 2013;57(6):2427–2435. PMID:22996424 DOI:10.1002/hep.26070
58. Fauconnet P., Klopfenstein C.E., Schiffer E. Hepatopulmonary syndrome: the anaesthetic considerations. Eur J Anaesthesiol. 2013;30(12):721–730. PMID:24161936 DOI:10.1097/EJA.0b013e328365bb6f
59. Gomez F.P., Martínez-Pallí G., Barberà J.A., et al. Gas exchange mechanism of orthodeoxia in hepatopulmonary syndrome. Hepatology. 2004;40(3):660–666. PMID:15349905 DOI:10.1002/hep.20358
60. Udoji T.N., Berkowitz D.M., Bechara R.I., et al. The use of transtracheal oxygen therapy in the management of severe hepatopulmonary syndrome after liver transplantation. Transplant Proc. 2013;45(9):3316–3319. PMID:24182809 DOI:10.1016/j.transproceed.2013.05.007
61. Nayyar D., Man H.S., Granton J., et al. Proposed management algorithm for severe hypoxemia after liver transplantation in the hepatopulmonary syndrome. Am J Transplant. 2015;15(4):903–913. PMID:25649047 DOI:10.1111/ajt.13177.
62. Alexander J., Greenough A., Baker A., et al. Nitric oxide treatment of severe hypoxemia after liver transplantation in hepatopulmonary syndrome: case report. Liver Transpl Surg. 1997;3(1):54–55. PMID:9377759
63. Schiller O., Avitzur Y., Kadmon G., et al. Nitric oxide for post- livertransplantation hypoxemia in pediatric hepatopulmonary syndrome: case report and review. Pediatr Transplant. 2011;15(7):E130–134. PMID:20408994 DOI:10.1111/j.1399-3046.2010.01313.x
64. Auzinger G., Willars C., Loveridge R., et al. Extracorporeal membrane oxygenation for refractory hypoxemia after liver transplantation in severe hepatopulmonary syndrome: a solution with pitfalls. Liver Transpl. 2014;20(9):1141– 1144. PMID:24916167 DOI:10.1002/lt.23926
65. Park T.J., Ahn K.S., Kim Y.H., et al. Improved severe hepatopulmonary syndrome after liver transplantation in an adolescent with end-stage liver disease secondary to biliary atresia. Clin Mol Hepatol. 2014;20(1):76–80. PMID:24757662 DOI:10.3350/cmh.2014.20.1.76
66. Taille C., Cadranel J., Bellocq A., et al. Liver transplantation for hepatopulmonary syndrome: a ten-year experience in Paris, France. Transplantation. 2003;75(9):1482–1489. PMID:12792501 DOI:10.1097/01.TP.0000061612.78954.6C
67. Arguedas M.R., Abrams G.A., Krowka M.J., Fallon M.B. Prospective evaluation of outcomes and predictors of mortality in patients with hepatopulmonary syndrome undergoing liver transplantation. Hepatology. 2003;37(1):192–197. PMID:12500204 DOI:10.1053/jhep.2003.50023
68. Krowka M.J., Mandell M.S., Ramsay M.A., et al. Hepatopulmonary syndrome and portopulmonary hypertension: a report of the multicenter liver transplant database. Liver Transpl. 2004;10(2):174–182. PMID:14762853 DOI:10.1002/lt.20016
69. Swanson K.L., Wiesner R.H., Krowka M.J. Natural history of hepatopulmonary syndrome: Impact of liver transplantation. Hepatology. 2005;41(5):1122–1129. PMID:15828054 DOI:10.1002/hep.20658
70. Deberaldini M., Arcanjo A.B., Melo E. Hepatopulmonary syndrome: morbidity and survival after liver transplantation. Transplant Proc. 2008;40(10):3512–3516. PMID:19100426 DOI:10.1016/j.transproceed.2008.08.134
71. Gupta S., Castel H., Rao R.V., et al. Improved survival after liver transplantation in patients with hepatopulmonary syndrome. Am J Transplant. 2010;10(2):354–363. PMID:19775311 DOI: 10.1111/j.1600-6143.2009.02822.x
Review
For citations:
Malinovskaya Yu.O., Dzhiner D., Ostroumov E.N., Moysyuk Ya.G. Hepatopulmonary syndrome and liver transplantation: the review and a case report. Transplantologiya. The Russian Journal of Transplantation. 2017;9(1):23-34. https://doi.org/10.23873/2074-0506-2017-9-1-23-34
Views:
1372
