Korean J Gastroenterol.  2023 Nov;82(5):213-223. 10.4166/kjg.2023.123.

Pulmonary Complications in Patients with Liver Cirrhosis

Affiliations
  • 1Department of Internal Medicine, Yonsei University Wonju College of Medicine, Wonju, Korea
  • 2Cell Therapy and Tissue Engineering Center, Yonsei University Wonju College of Medicine, Wonju, Korea
  • 3Regeneration Medicine Research Center, Yonsei University Wonju College of Medicine, Wonju, Korea

Abstract

Portal hypertension is a clinical syndrome defined by an increased portal venous pressure. The most frequent cause of portal hypertension is liver cirrhosis, and many of the complications of cirrhosis, such as ascites and gastroesophageal variceal bleeding, are related to portal hypertension. Portal hypertension is a pathological condition caused by the accumulation of blood flow in the portal system. This blood flow retention reduces the effective circulation volume. To compensate for these changes, neurotransmitter hormone changes and metabolic abnormalities occur, which cause complications in organs other than the liver. A hepatic hydrothorax is fluid accumulation in the pleural space resulting from increased portal pressure. Hepatopulmonary syndrome and portopulmonary hypertension are the pulmonary complications in cirrhosis by deforming the vascular structure. Symptoms, such as dyspnea and hypoxia, affect the survival and the quality of life of patients. These lung complications are usually underestimated in the management of cirrhosis. This review briefly introduces the type of lung complications of cirrhosis.

Keyword

Liver cirrhosis; Portal hypertension; Hydrothorax; Hepatopulmonary syndrome; Pulmonary hypertension

Reference

1. Chaaban T, Kanj N, Bou Akl I. 2019; Hepatic hydrothorax: An updated review on a challenging disease. Lung. 197:399–405. DOI: 10.1007/s00408-019-00231-6. PMID: 31129701.
2. Banini BA, Alwatari Y, Stovall M, et al. Multidisciplinary management of hepatic hydrothorax in 2020: An evidence-based review and guidance. Hepatology. 2020; 72:1851–1863. DOI: 10.1002/hep.31434. PMID: 32585037.
Article
3. Matono T, Koda M, Murawaki Y. 2012; Right diaphragmatic defect in hepatic hydrothorax exposed by contrast-enhanced ultrasonography after radiofrequency ablation. Hepatology. 56:784–785. DOI: 10.1002/hep.25860. PMID: 22618966.
Article
4. Mücke VT, Fitting D, Dultz G, et al. 2022; Application of contrast-enhanced ultrasound to detect hepatic hydrothorax in patients with liver cirrhosis. Ultraschall Med. 43:473–478. DOI: 10.1055/a-1189-2937. PMID: 32674185.
Article
5. Gurung P, Goldblatt M, Huggins JT, Doelken P, Nietert PJ, Sahn SA. 2011; Pleural fluid analysis and radiographic, sonographic, and echocardiographic characteristics of hepatic hydrothorax. Chest. 140:448–453. DOI: 10.1378/chest.10-2134. PMID: 21273292. PMCID: PMC3148794.
Article
6. Lv Y, Han G, Fan D. 2018; Hepatic hydrothorax. Ann Hepatol. 17:33–46. DOI: 10.5604/01.3001.0010.7533. PMID: 29311408.
Article
7. Mohamed A, Atef M, Alsebaey A, Musa Elhabshy M, Salama M. 2017; Combined spontaneous bacterial empyema and peritonitis in cirrhotic patients with ascites and hepatic hydrothorax. Arab J Gastroenterol. 18:104–107. DOI: 10.1016/j.ajg.2017.05.010. PMID: 28579346.
Article
8. Makhlouf HA, Morsy KH, Makhlouf NA, Eldin EN, Khairy M. 2013; Spontaneous bacterial empyema in patients with liver cirrhosis in Upper Egypt: prevalence and causative organisms. Hepatol Int. 7:274–279. DOI: 10.1007/s12072-012-9372-5. PMID: 26201642.
Article
9. Xiol X, Castellote J, Baliellas C, et al. 1990; Spontaneous bacterial empyema in cirrhotic patients: analysis of eleven cases. Hepatology. 11:365–370. DOI: 10.1002/hep.1840110306. PMID: 2179097.
Article
10. Xiol X, Castellví JM, Guardiola J, et al. 1996; Spontaneous bacterial empyema in cirrhotic patients: a prospective study. Hepatology. 23:719–723. DOI: 10.1002/hep.510230410. PMID: 8666323.
Article
11. Chen CH, Shih CM, Chou JW, et al. 2011; Outcome predictors of cirrhotic patients with spontaneous bacterial empyema. Liver Int. 31:417–424. DOI: 10.1111/j.1478-3231.2010.02447.x. PMID: 21281436.
Article
12. Korean Association for the Study of the Liver (KASL). 2018; KASL clinical practice guidelines for liver cirrhosis: Ascites and related complications. Clin Mol Hepatol. 24:230–277. DOI: 10.3350/cmh.2018.1005. PMID: 29991196. PMCID: PMC6166105.
13. Ryu JY, Baek SH, Kim S. 2023; Evidence-based hyponatremia management in liver disease. Clin Mol Hepatol. 29:924–944. DOI: 10.3350/cmh.2023.0090. PMID: 37280091. PMCID: PMC10577348.
Article
14. Wong F. 2023; Management of refractory ascites. Clin Mol Hepatol. 29:16–32. DOI: 10.3350/cmh.2022.0104. PMID: 35676862. PMCID: PMC9845666.
Article
15. Lee HL, Lee SW. 2022; The role of transjugular intrahepatic portosystemic shunt in patients with portal hypertension: Advantages and pitfalls. Clin Mol Hepatol. 28:121–134. DOI: 10.3350/cmh.2021.0239. PMID: 34571587. PMCID: PMC9013617.
Article
16. Kalambokis G, Fotopoulos A, Economou M, Pappas K, Tsianos EV. 2007; Effects of a 7-day treatment with midodrine in non-azotemic cirrhotic patients with and without ascites. J Hepatol. 46:213–221. DOI: 10.1016/j.jhep.2006.09.012. PMID: 17156883.
Article
17. Dumortier J, Leprêtre J, Scalone O, et al. 2000; Successful treatment of hepatic hydrothorax with octreotide. Eur J Gastroenterol Hepatol. 12:817–820. DOI: 10.1097/00042737-200012070-00018. PMID: 10929913.
Article
18. Ibrisim D, Cakaloglu Y, Akyuz F, et al. 2006; Treatment of hepatic hydrothorax with terlipressin in a cirrhotic patient. Scand J Gastroenterol. 41:862–865. DOI: 10.1080/00365520500527441. PMID: 16785202.
Article
19. Escorsell A, Bandi JC, Andreu V, et al. 2001; Desensitization to the effects of intravenous octreotide in cirrhotic patients with portal hypertension. Gastroenterology. 120:161–169. DOI: 10.1053/gast.2001.20892. PMID: 11208725.
Article
20. Sanyal AJ. 2001; Octreotide and its effects on portal circulation. Gastroenterology. 120:303–305. DOI: 10.1053/gast.2001.21619. PMID: 11208741.
Article
21. Xiol X, Castellote J, Cortes-Beut R, Delgado M, Guardiola J, Sesé E. 2001; Usefulness and complications of thoracentesis in cirrhotic patients. Am J Med. 111:67–69. DOI: 10.1016/S0002-9343(01)00744-6. PMID: 11448663.
Article
22. Shojaee S, Khalid M, Kallingal G, Kang L, Rahman N. 2018; Repeat thoracentesis in hepatic hydrothorax and non-hepatic hydrothorax effusions: A case-control study. Respiration. 96:330–337. DOI: 10.1159/000490001. PMID: 29991046.
Article
23. Hung TH, Tseng CW, Tsai CC, Hsieh YH, Tseng KC, Tsai CC. 2017; Mortality following catheter drainage versus thoracentesis in cirrhotic patients with pleural effusion. Dig Dis Sci. 62:1080–1085. DOI: 10.1007/s10620-017-4463-8. PMID: 28130709.
Article
24. Ridha A, Al-Abboodi Y, Fasullo M. 2017; The outcome of thoracentesis versus chest tube placement for hepatic hydrothorax in patients with cirrhosis: A nationwide analysis of the national inpatient sample. Gastroenterol Res Pract. 2017:5872068. DOI: 10.1155/2017/5872068. PMID: 29317865. PMCID: PMC5727694.
Article
25. Chen A, Massoni J, Jung D, Crippin J. 2016; Indwelling tunneled pleural catheters for the management of hepatic hydrothorax. A pilot study. Ann Am Thorac Soc. 13:862–866. DOI: 10.1513/AnnalsATS.201510-688BC. PMID: 27015392.
Article
26. Han SK, Kang SH, Kim MY, et al. 2022; Outcome of intermittent thoracentesis versus pigtail catheter drainage for hepatic hydrothorax. J Clin Med. 11:7221. DOI: 10.3390/jcm11237221. PMID: 36498795. PMCID: PMC9735472.
Article
27. Ditah IC, Al Bawardy BF, Saberi B, Ditah C, Kamath PS. 2015; Transjugular intrahepatic portosystemic stent shunt for medically refractory hepatic hydrothorax: A systematic review and cumulative meta-analysis. World J Hepatol. 7:1797–1806. DOI: 10.4254/wjh.v7.i13.1797. PMID: 26167253. PMCID: PMC4491909.
Article
28. Dhanasekaran R, West JK, Gonzales PC, et al. 2010; Transjugular intrahepatic portosystemic shunt for symptomatic refractory hepatic hydrothorax in patients with cirrhosis. Am J Gastroenterol. 105:635–641. DOI: 10.1038/ajg.2009.634. PMID: 19904245.
Article
29. Perarnau JM, Le Gouge A, Nicolas C, et al. 2014; Covered vs. uncovered stents for transjugular intrahepatic portosystemic shunt: a randomized controlled trial. J Hepatol. 60:962–968. DOI: 10.1016/j.jhep.2014.01.015. PMID: 24480619.
Article
30. Parker R, Armstrong MJ, Rowe IA, Houlihan DD. 2013; Estimated short-term mortality following TIPS insertion for patients with hepatic hydrothorax. Am J Gastroenterol. 108:1806–1807. DOI: 10.1038/ajg.2013.290. PMID: 24192954.
Article
31. Hou F, Qi X, Guo X. 2016; Effectiveness and safety of pleurodesis for hepatic hydrothorax: A systematic review and meta-analysis. Dig Dis Sci. 61:3321–3334. DOI: 10.1007/s10620-016-4260-9. PMID: 27456504.
Article
32. Milanez de Campos JR, Filho LO, de Campos Werebe E, et al. 2000; Thoracoscopy and talc poudrage in the management of hepatic hydrothorax. Chest. 118:13–17. DOI: 10.1378/chest.118.1.13. PMID: 10893352.
Article
33. Huang PM, Kuo SW, Chen JS, Lee JM. 2016; Thoracoscopic mesh repair of diaphragmatic defects in hepatic hydrothorax: A 10-year experience. Ann Thorac Surg. 101:1921–1927. DOI: 10.1016/j.athoracsur.2015.11.023. PMID: 26897323.
Article
34. Xiol X, Tremosa G, Castellote J, et al. 2005; Liver transplantation in patients with hepatic hydrothorax. Transpl Int. 18:672–675. DOI: 10.1111/j.1432-2277.2005.00116.x. PMID: 15910292.
Article
35. Endo K, Iida T, Yagi S, et al. 2014; Impact of preoperative uncontrollable hepatic hydrothorax and massive ascites in adult liver transplantation. Surg Today. 44:2293–2299. DOI: 10.1007/s00595-014-0839-y. PMID: 24509883.
Article
36. Hung TH, Tseng CW, Tsai CC, Tsai CC, Tseng KC, Hsieh YH. 2018; The long-term outcomes of cirrhotic patients with pleural effusion. Saudi J Gastroenterol. 24:46–51. DOI: 10.4103/sjg.SJG_336_17. PMID: 29451184. PMCID: PMC5848324.
Article
37. Raevens S, Boret M, Fallon MB. 2022; Hepatopulmonary syndrome. JHEP Rep. 4:100527. DOI: 10.1016/j.jhepr.2022.100527. PMID: 36035361. PMCID: PMC9403489.
Article
38. Machicao VI, Balakrishnan M, Fallon MB. 2014; Pulmonary complications in chronic liver disease. Hepatology. 59:1627–1637. DOI: 10.1002/hep.26745. PMID: 24089295.
Article
39. Krowka MJ, Fallon MB, Kawut SM, et al. 2016; International liver transplant society practice guidelines: Diagnosis and management of hepatopulmonary syndrome and portopulmonary hypertension. Transplantation. 100:1440–1452. DOI: 10.1097/TP.0000000000001229. PMID: 27326810.
40. Abrams GA, Jaffe CC, Hoffer PB, Binder HJ, Fallon MB. 1995; Diagnostic utility of contrast echocardiography and lung perfusion scan in patients with hepatopulmonary syndrome. Gastroenterology. 109:1283–1288. DOI: 10.1016/0016-5085(95)90589-8. PMID: 7557096.
Article
41. Suk KT, Kim MY, Jeong SW, Jang JY, Jang YO, Baik SK. 2018; Impact of bacterial translocation on hepatopulmonary syndrome: A prospective observational study. Dig Dis Sci. 63:248–256. DOI: 10.1007/s10620-017-4868-4. PMID: 29192374.
Article
42. Meristoudis G, Keramida G, Ilias I. 2020; Lung perfusion imaging with technetium-99m macroaggregated albumin should be combined with contrast-enhanced echocardiography for the diagnosis of hepatopulmonary syndrome. Mol Imaging Radionucl Ther. 29:143–144. DOI: 10.4274/mirt.galenos.2020.52244. PMID: 33094580. PMCID: PMC7583746.
Article
43. Nunes H, Lebrec D, Mazmanian M, et al. 2001; Role of nitric oxide in hepatopulmonary syndrome in cirrhotic rats. Am J Respir Crit Care Med. 164:879–885. DOI: 10.1164/ajrccm.164.5.2009008. PMID: 11549549.
Article
44. Liu L, Zhang M, Luo B, Abrams GA, Fallon MB. 2001; Biliary cyst fluid from common bile duct-ligated rats stimulates endothelial nitric oxide synthase in pulmonary artery endothelial cells: a potential role in hepatopulmonary syndrome. Hepatology. 33:722–727. DOI: 10.1053/jhep.2001.22701. PMID: 11230754.
Article
45. Hoeper MM, Krowka MJ, Strassburg CP. 2004; Portopulmonary hypertension and hepatopulmonary syndrome. Lancet. 363:1461–1468. DOI: 10.1016/S0140-6736(04)16107-2. PMID: 15121411.
Article
46. Krowka MJ, Wiseman GA, Burnett OL, et al. 2000; Hepatopulmonary syndrome: a prospective study of relationships between severity of liver disease, PaO2 response to 100% oxygen, and brain uptake after 99mTc MAA lung scanning. Chest. 118:615–624. DOI: 10.1378/chest.118.3.615. PMID: 10988181.
47. Fallon MB, Krowka MJ, Brown RS, et al. 2008; Impact of hepatopulmonary syndrome on quality of life and survival in liver transplant candidates. Gastroenterology. 135:1168–1175. DOI: 10.1053/j.gastro.2008.06.038. PMID: 18644373. PMCID: PMC2824882.
Article
48. Han SK, Kim MY, Kang SH, Suk KT, Baik SK. 2021; Hepatopulmonary syndrome is related to the development of acute-on-chronic liver failure and poor prognosis in cirrhotic patients. Hepatol Int. 15:1207–1214. DOI: 10.1007/s12072-021-10226-2. PMID: 34319553.
Article
49. Fallon MB, Mulligan DC, Gish RG, Krowka MJ. 2006; Model for end-stage liver disease (MELD) exception for hepatopulmonary syndrome. Liver Transpl. 12(12 Suppl 3):S105–S107. DOI: 10.1002/lt.20971. PMID: 17123282.
Article
50. Swanson KL, Wiesner RH, Krowka MJ. 2005; Natural history of hepatopulmonary syndrome: Impact of liver transplantation. Hepatology. 41:1122–1129. DOI: 10.1002/hep.20658. PMID: 15828054.
Article
51. Arguedas MR, Abrams GA, Krowka MJ, Fallon MB. 2003; Prospective evaluation of outcomes and predictors of mortality in patients with hepatopulmonary syndrome undergoing liver transplantation. Hepatology. 37:192–197. DOI: 10.1053/jhep.2003.50023. PMID: 12500204.
Article
52. Goldberg DS, Krok K, Batra S, Trotter JF, Kawut SM, Fallon MB. 2014; Impact of the hepatopulmonary syndrome MELD exception policy on outcomes of patients after liver transplantation: an analysis of the UNOS database. Gastroenterology. 146:1256–1265.e1. DOI: 10.1053/j.gastro.2014.01.005. PMID: 24412528. PMCID: PMC3992191.
Article
53. Grady K, Gowda S, Kingah P, Soubani AO. 2015; Coil embolization of pulmonary arteries as a palliative treatment of diffuse type I hepatopulmonary syndrome. Respir Care. 60:e20–e25. DOI: 10.4187/respcare.03198. PMID: 25185147.
Article
54. Hadengue A, Benhayoun MK, Lebrec D, Benhamou JP. 1991; Pulmonary hypertension complicating portal hypertension: prevalence and relation to splanchnic hemodynamics. Gastroenterology. 100:520–528. DOI: 10.1016/0016-5085(91)90225-A. PMID: 1985048.
Article
55. Krowka MJ. 2012; Portopulmonary hypertension. Semin Respir Crit Care Med. 33:17–25. DOI: 10.1055/s-0032-1301731. PMID: 22447257.
Article
56. Thomas C, Glinskii V, de Jesus Perez V, Sahay S. 2020; Portopulmonary hypertension: From bench to bedside. Front Med (Lausanne). 7:569413. DOI: 10.3389/fmed.2020.569413. PMID: 33224960. PMCID: PMC7670077.
57. Huertas A, Guignabert C, Barberà JA, et al. 2018; Pulmonary vascular endothelium: the orchestra conductor in respiratory diseases: Highlights from basic research to therapy. Eur Respir J. 51:1700745. DOI: 10.1183/13993003.00745-2017. PMID: 29545281.
58. Shenoda B, Boselli J. 2019; Vascular syndromes in liver cirrhosis. Clin J Gastroenterol. 12:387–397. DOI: 10.1007/s12328-019-00956-0. PMID: 30980261.
Article
59. Desroches-Castan A, Tillet E, Ricard N, et al. 2019; Bone morphogenetic protein 9 is a paracrine factor controlling liver sinusoidal endothelial cell fenestration and protecting against hepatic fibrosis. Hepatology. 70:1392–1408. DOI: 10.1002/hep.30655. PMID: 30964206.
Article
60. Long L, Ormiston ML, Yang X, et al. 2015; Selective enhancement of endothelial BMPR-II with BMP9 reverses pulmonary arterial hypertension. Nat Med. 21:777–785. DOI: 10.1038/nm.3877. PMID: 26076038. PMCID: PMC4496295.
Article
61. Jonigk D, Golpon H, Bockmeyer CL, et al. 2011; Plexiform lesions in pulmonary arterial hypertension composition, architecture, and microenvironment. Am J Pathol. 179:167–179. DOI: 10.1016/j.ajpath.2011.03.040. PMID: 21703400. PMCID: PMC3123793.
62. Simonneau G, Montani D, Celermajer DS, et al. 2019; Haemodynamic definitions and updated clinical classification of pulmonary hypertension. Eur Respir J. 53:1801913. DOI: 10.1183/13993003.01913-2018. PMID: 30545968. PMCID: PMC6351336.
Article
63. Kim WR, Krowka MJ, Plevak DJ, et al. 2000; Accuracy of Doppler echocardiography in the assessment of pulmonary hypertension in liver transplant candidates. Liver Transpl. 6:453–458. DOI: 10.1053/jlts.2000.7573. PMID: 10915168.
Article
64. Martin P, DiMartini A, Feng S, Brown R Jr, Fallon M. 2014; Evaluation for liver transplantation in adults: 2013 practice guideline by the American Association for the Study of Liver Diseases and the American Society of Transplantation. Hepatology. 59:1144–1165. DOI: 10.1002/hep.26972. PMID: 24716201.
Article
65. Cartin-Ceba R, Halank M, Ghofrani HA, et al. 2018; Riociguat treatment for portopulmonary hypertension: a subgroup analysis from the PATENT-1/-2 studies. Pulm Circ. 8:2045894018769305. DOI: 10.1177/2045894018769305. PMID: 29565224. PMCID: PMC5987907.
66. Soulaidopoulos S, Goulis I, Cholongitas E. 2020; Pulmonary manifestations of chronic liver disease: a comprehensive review. Ann Gastroenterol. 33:237–249. DOI: 10.20524/aog.2020.0474. PMID: 32382226. PMCID: PMC7196609.
Article
67. DuBrock HM, Goldberg DS, Sussman NL, et al. 2017; Predictors of waitlist mortality in portopulmonary hypertension. Transplantation. 101:1609–1615. DOI: 10.1097/TP.0000000000001666. PMID: 28207639. PMCID: PMC5481480.
Article
68. Krowka MJ, Plevak DJ, Findlay JY, Rosen CB, Wiesner RH, Krom RA. 2000; Pulmonary hemodynamics and perioperative cardiopulmonary-related mortality in patients with portopulmonary hypertension undergoing liver transplantation. Liver Transpl. 6:443–450. DOI: 10.1053/jlts.2000.6356. PMID: 10915166.
Article
69. Savale L, Sattler C, Coilly A, et al. 2017; Long-term outcome in liver transplantation candidates with portopulmonary hypertension. Hepatology. 65:1683–1692. DOI: 10.1002/hep.28990. PMID: 27997987.
Article
70. Li J, Zhuang Q, Zhang X, et al. 2018; Prevalence and prognosis of portopulmonary hypertension in 223 liver transplant recipients. Can Respir J. 2018:9629570. DOI: 10.1155/2018/9629570. PMID: 30319722. PMCID: PMC6167565.
Article
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