Intestinal endotoxemia plays a central role in development of hepatopulmonary syndrome in a cirrhotic rat model induced by multiple pathogenic factors

World Journal of Gastroenterology

Volumn 13, Issue 47, 2007, Pages 6385-6395

  Zhang, Hui Ying ^a   Han, De Wu ^b   Su, Ai Rong ^c   Zhang, Li Tong ^d   Zhao, Zhong Fu ^a   Ji, Jing Quan ^a   Li, Bao Hong ^a   Ji, Cheng ^e  

^a CHANGZHI MEDICAL COLLEGE   (China)

^b SHANXI MEDICAL UNIVERSITY   (China)

^c BENGBU MEDICAL COLLEGE   (China)

^d Shanxi Modern Women Hospital   (China)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Alcohol; Capillary; Cirrhosis; Endotoxin; Hemeoxygenase 1; Hepatopulmonary syndrome; Nacrophage; Nitric oxide synthase

Indexed keywords

ALANINE AMINOTRANSFERASE; AMINOGUANIDINE; CARBON MONOXIDE; CARBON TETRACHLORIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPOLYSACCHARIDE; MALONALDEHYDE; MESSENGER RNA; N(G) NITROARGININE METHYL ESTER; NITRATE; NITRIC OXIDE SYNTHASE INHIBITOR; NITRITE; PROTOPORPHYRIN ZINC;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; DISEASE COURSE; DISEASE SEVERITY; ENDOTOXEMIA; HEPATOPULMONARY SYNDROME; HISTOPATHOLOGY; LIVER CIRRHOSIS; LIVER DYSFUNCTION; LUNG ALVEOLUS MACROPHAGE; LUNG CAPILLARY; LUNG LAVAGE; MALE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; PATHOGENESIS; PORTAL HYPERTENSION; PORTAL VEIN BLOOD PRESSURE; PROTEIN EXPRESSION; RAT; RISK ASSESSMENT; RISK FACTOR; VASODILATATION;

EID: 37648998870     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.v13.i47.6385     Document Type: Article

References (64)

1. Rodriguez-Roisin R, Krowka MJ, Herve P, Fallon MB. Pulmonary-Hepatic vascular Disorders (PHD). Eur Respir J 2004; 24: 861-880
2. Schenk P, Schoniger-Hekele M, Fuhrmann V, Madl C, Silberhumer G, Muller C. Prognostic significance of the hepatopulmonary syndrome in patients with cirrhosis. Gastroenterology 2003; 125: 1042-1052
3. Swanson KL, Wiesner RH, Krowka MJ. Natural history of hepatopulmonary syndrome: Impact of liver transplantation. Hepatology 2005; 41: 1122-1129
4. Cremona G, Higenbottam TW, Mayoral V, Alexander G, Demoncheaux E, Borland C, Roe P, Jones GJ. Elevated exhaled nitric oxide in patients with hepatopulmonary syndrome. Eur Respir J 1995; 8: 1883-1885
5. Rolla G, Brussino L, Colagrande P, Scappaticci E, Morello M, Bergerone S, Ottobrelli A, Cerutti E, Polizzi S, Bucca C. Exhaled nitric oxide and impaired oxygenation in cirrhotic patients before and after liver transplantation. Ann Intern Med 1998; 129: 375-378
6. Rolla G, Bucca C, Brussino L. Methylene blue in the hepatopulmonary syndrome. N Engl J Med 1994; 331: 1098
7. Brussino L, Bucca C, Morello M, Scappaticci E, Mauro M, Rolla G. Effect on dyspnoea and hypoxaemia of inhaled N(G)-nitro-L-arginine methyl ester in hepatopulmonary syndrome. Lancet 2003; 362: 43-44
8. Schenk P, Madl C, Rezaie-Majd S, Lehr S, Muller C. Methylene blue improves the hepatopulmonary syndrome. Ann Intern Med 2000; 133: 701-706
9. Gomez FP, Barbera JA, Roca J, Burgos F, Gistau C, Rodriguez-Roisin R. Effects of nebulized N(G)-nitro-L-arginine methyl ester in patients with hepatopulmonary syndrome. Hepatology 2006; 43: 1084-1091
10. Almeida JA, Riordan SM, Liu J, Galhenage S, Kim R, Bihari D, Wegner EA, Cranney GB, Thomas PS. Deleterious effect of nitric oxide inhibition in chronic hepatopulmonary syndrome. Eur J Gastroenterol Hepatol 2007; 19: 341-346
11. Arguedas MR, Drake BB, Kapoor A, Fallon MB. Carboxyhemoglobin levels in cirrhotic patients with and without hepatopulmonary syndrome. Gastroenterology 2005; 128: 328-333
12. Cody CS and DL Dunn. Endotoxins and septic shock. In: Handbook of Mediators in Septic Shock, edited by Neugebauer EA, and Holady JW. Boca Raton, FL: CRC Press, 1993: 1-38
13. Vito L, Dennis RC, Weisel RD, Hechtman HB. Sepsis presenting as acute respiratory insufficiency. Surg Gynecol Obstet 1974; 138: 896-900
14. Zhao LF, Han DW. Clinical significance of endotoxemia in patients with liver disease. Shijie Huaren Xiaohua Zazhi 1999; 7: 391-393
15. Liu JC, Han DW and Wang R. Influence of endothelin on renal function in rats with cirrhosis. Zhongguo Binglishengli Zazhi 1998; 14: 717-719
16. Wang R, Han DW, Liu JC and Zhao YC. Studies on the pathogenesis of renal insufficiency in acute hepatic failure. Zhongguo Binglishengli Zazhi 1999; 7: 482-486
17. Wang R, Liu JC, Han DW and Zhao YC. The dynamic changes of renal LTC4 in acute hepatic failure. Zhongguo Binglishengli Zazhi 1998; 14: 720-722
18. Wang R, Liu JC and Han DW. Eddects of endothelin on renal insufficiency in acute hepatic failure. Zhongguo Binglishengli Zazhi 1999; 15: 154-156
19. Li XQ, Han DW, Xu RL, Zhao YC, MA XH. Hepatic encephalopathy in cirrhotic rats induced by endotoxin injection. Zhongguo Binglishengli Zazhi 1999; 15: 151-153
20. Zhang HY, Han DW, Zhao ZF, Liu MS, Wu YJ, Chen XM, Ji C. Multiple pathogenic factor-induced complications of cirrhosis in rats: a new model of hepatopulmonary syndrome with intestinal endotoxemia. World J Gastroenterol 2007; 13: 3500-3507
21. MacPhail CM, Monnet E, Gaynor JS. Evaluation of splanchnic oxygen extraction ratio as an index of portal vein pressure in dogs. Am J Vet Res 2002; 63: 15-18
22. Murphy PR, Limoges M, Dodd F, Boudreau RT, Too CK. Fibroblast growth factor-2 stimulates endothelial nitric oxide synthase expression and inhibits apoptosis by a nitric oxide-dependent pathway in Nb2 lymphoma cells. Endocrinology 2001; 142: 81-88
23. Wu F, Park F, Cowley AW Jr, Mattson DL. Quantification of nitric oxide synthase activity in microdissected segments of the rat kidney. Am J Physiol 1999; 276: F874-F881
24. Nanji AA, Miao L, Thomas P, Rahemtulla A, Khwaja S, Zhao S, Peters D, Tahan SR, Dannenberg AJ. Enhanced cyclooxygenase-2 gene expression in alcoholic liver disease in the rat. Gastroenterology 1997; 112: 943-951
25. Schenk P, Fuhrmann V, Madl C, Funk G, Lehr S, Kandel O, Muller C. Hepatopulmonary syndrome: prevalence and predictive value of various cut offs for arterial oxygenation and their clinical consequences. Gut 2002; 51: 853-859
26. Martinez GP, Barbera JA, Visa J, Rimola A, Pare JC, Roca J, Navasa M, Rodes J, Rodriguez-Roisin R. Hepatopulmonary syndrome in candidates for liver transplantation. J Hepatol 2001; 34: 651-657
27. Abrams GA, Jaffe CC, Hoffer PB, Binder HJ, Fallon MB. Diagnostic utility of contrast echocardiography and lung perfusion scan in patients with hepatopulmonary syndrome. Gastroenterology 1995; 109: 1283-1288
28. Krowka MJ, Wiseman GA, Burnett OL, Spivey JR, Therneau T, Porayko MK, Wiesner RH. Hepatopulmonary syndrome: a prospective study of relationships between severity of liver disease, PaO(2) response to 100% oxygen, and brain uptake after (99m)Tc MAA lung scanning. Chest 2000; 118: 615-624
29. Whyte MK, Hughes JM, Peters AM, Ussov W, Patel S, Burroughs AK. Analysis of intrapulmonary right to left shunt in the hepatopulmonary syndrome. J Hepatol 1998; 29: 85-93
30. Regev A, Yeshurun M, Rodriguez M, Sagie A, Neff GW, Molina EG, Schiff ER. Transient hepatopulmonary syndrome in a patient with acute hepatitis A. J Viral Hepat 2001; 8: 83-86
31. Silverman A, Cooper MD, Moller JH, Good RA. Syndrome of cyanosis, digital clubbing, and hepatic disease in siblings. J Pediatr 1968; 72: 70-80
32. Teuber G, Teupe C, Dietrich CF, Caspary WF, Buhl R, Zeuzem S. Pulmonary dysfunction in non-cirrhotic patients with chronic viral hepatitis. Eur J Intern Med 2002; 13: 311-318
33. Fuhrmann V, Madl C, Mueller C, Holzinger U, Kitzberger R, Funk GC, Schenk P. Hepatopulmonary syndrome in patients with hypoxic hepatitis. Gastroenterology 2006; 131: 69-75
34. Gupta D, Vijaya DR, Gupta R, Dhiman RK, Bhargava M, Verma J, Chawla YK. Prevalence of hepatopulmonary syndrome in cirrhosis and extrahepatic portal venous obstruction. Am J Gastroenterol 2001; 96: 3395-3399
35. De BK, Sen S, Biswas PK, Sanyal R, Jumdar DM, Biswas J. Hepatopulmonary syndrome in inferior vena cava obstruction responding to cavoplasty. Gastroenterology 2000; 118: 192-196
36. Berthelot P, Walker JG, Sherlock S, Reid L. Arterial changes in the lungs in cirrhosis of the liver - lung spider nevi. N Engl J Med 1966; 274: 291-298
37. Rodriguez-Roisin R, Roca J, Agusti AG, Mastai R, Wagner PD, Bosch J. Gas exchange and pulmonary vascular reactivity in patients with liver cirrhosis. Am Rev Respir Dis 1987; 135: 1085-1092
38. Melot C, Naeije R, Dechamps P, Hallemans R, Lejeune P. Pulmonary and extrapulmonary contributors to hypoxemia in liver cirrhosis. Am Rev Respir Dis 1989; 139: 632-640
39. Hedenstierna G, Soderman C, Eriksson LS, Wahren J. Ventilation-perfusion inequality in patients with non-alcoholic liver cirrhosis. Eur Respir J 1991; 4: 711-717
40. Thorens JB, Junod AF. Hypoxaemia and liver cirrhosis: a new argument in favour of a " diffusion-perfusion defect". Eur Respir J 1992; 5: 754-756
41. Crawford AB, Regnis J, Laks L, Donnelly P, Engel LA, Young IH. Pulmonary vascular dilatation and diffusion-dependent impairment of gas exchange in liver cirrhosis. Eur Respir J 1995; 8: 2015-2021
42. Krowka MJ, Porayko MK, Plevak DJ, Pappas SC, Steers JL, Krom RA, Wiesner RH. Hepatopulmonary syndrome with progressive hypoxemia as an indication for liver transplantation: case reports and literature review. Mayo Clin Proc 1997; 72: 44-53
43. Rodrignez-Roisin R, Agusti AG, Roca J. The hepatopulmonary syndrome: new name, old complexities. Thorax 1992; 47: 897-902
44. Schraufnagel DE, Malik R, Goel V, Ohara N, Chang SW. Lung capillary changes in hepatic cirrhosis in rats. Am J Physiol 1997; 272: L139-L147
45. Lee J, Menkis AH, Rosenberg HC. Reversal of pulmonary arteriovenous malformation after diversion of anomalous hepatic drainage. Ann Thorac Surg 1998; 65: 848-849
46. Alvarez AE, Ribeiro AF, Hessel G, Baracat J, Ribeiro JD. Abernethy malformation: one of the etiologies of hepatopulmonary syndrome. Pediatr Pulmonol 2002; 34: 391-394
47. Eriksson LS, Soderman C, Ericzon BG, Eleborg L, Wahren J, Hedenstierna G. Normalization of ventilation/perfusion relationships after liver transplantation in patients with decompensated cirrhosis: evidence for a hepatopulmonary syndrome. Hepatology 1990; 12: 1350-1357
48. Vallance P, Moncada S. Hyperdynamic circulation in cirrhosis: a role for nitric oxide? Lancet 1991; 337: 776-778
49. Rolla G. Is nitric oxide the ultimate mediator in hepatopulmonary syndrome? J Hepatol 2003; 38: 668-670
50. Fallon MB, Abrams GA, Luo B, Hou Z, Dai J, Ku DD. The role of endothelial nitric oxide synthase in the pathogenesis of a rat model of hepatopulmonary syndrome. Gastroenterology 1997; 113: 606-614
51. Luo B, Abrams GA, Fallon MB. Endothelin-1 in the rat bile duct ligation model of hepatopulmonary syndrome: correlation with pulmonary dysfunction. J Hepatol 1998; 29: 571-578
52. Zhang J, Ling Y, Luo B, Tang L, Ryter SW, Stockard CR, Grizzle WE, Fallon MB. Analysis of pulmonary heme oxygenase-1 and nitric oxide synthase alterations in experimental hepatopulmonary syndrome. Gastroenterology 2003; 125: 1441-1451
53. Nunes H, Lebrec D, Mazmanian M, Capron F, Heller J, Tazi KA, Zerbib E, Dulmet E, Moreau R, Dinh-Xuan AT, Simormeau G, Herve P. Role of nitric oxide in hepatopulmonary syndrome in cirrhotic rats. Am J Respir Crit Care Med 2001; 164: 879-885
54. Shweiki D, Itin A, Softer D, Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 1992; 359: 843-845
55. Risau W. Mechanisms of angiogenesis. Nature 1997; 386: 671-674
56. Shaul PW, North AJ, Brannon TS, Ujiie K, Wells LB, Nisen PA, Lowenstein CJ, Snyder SH, Star RA. Prolonged in vivo hypoxia enhances nitric oxide synthase type I and type III gene expression in adult rat lung. Am J Respir Cell Mol Biol 1995; 13: 167-174
57. Melillo G, Musso T, Sica A, Taylor LS, Cox GW, Varesio L. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 1995; 182: 1683-1693
58. Coulet F, Nadaud S, Agrapart M, Soubrier F. Identification of hypoxia-response element in the human endothelial nitric-oxide synthase gene promoter. J Biol Chem 2003; 278: 46230-46240
59. Hood JD, Meininger CJ, Ziche M, Granger HJ. VEGF upregulates ecNOS message, protein, and NO production in human endothelial cells. Am J Physiol 1998; 274: H1054-H1058
60. Papapetropoulos A, Garcia-Cardena G, Madri JA, Sessa WC. Nitric oxide production contributes to the angiogenic properties of vascular endothelial growth factor in human endothelial cells. J Clin Invest 1997; 100: 3131-3139
61. Uhlmann S, Friedrichs U, Eichler W, Hoffmann S, Wiedemann P. Direct measurement of VEGF-induced nitric oxide production by choroidal endothelial cells. Microvasc Res 2001; 62: 179-189
62. Ghiso N, Rohan RM, Amano S, Garland R, Adamis AP. Suppression of hypoxia-associated vascular endothelial growth factor gene expression by nitric oxide via cGMP. Invest Ophthalmol Vis Sci 1999; 40: 1033-1039
63. Sztrymf B, Rabiller A, Nunes H, Savale L, Lebrec D, Le Pape A, de Montpreville V, Mazmanian M, Humbert M, Herve P. Prevention of hepatopulmonary syndrome and hyperdynamic state by pentoxifylline in cirrhotic rats. Eur Respir J 2004; 23: 752-758
64. Rabiller A, Nunes H, Lebrec D, Tazi KA, Wartski M, Dulmet E, Libert JM, Mougeot C, Moreau R, Mazmanian M, Humbert M, Herve P. Prevention of gram-negative translocation reduces the severity of hepatopulmonary syndrome. Am J Respir Crit Care Med 2002; 166: 514-517