Hostname: page-component-6766d58669-l4t7p Total loading time: 0 Render date: 2026-05-18T20:33:48.476Z Has data issue: false hasContentIssue false
  • English
  • Français

Normal and abnormal pulmonary arteriovenous shunting: occurrence and mechanisms

Published online by Cambridge University Press:  05 March 2013

Julien I.E. Hoffman
Julien I.E. Hoffman*
Affiliation:
Department of Pediatrics, University of California, San Francisco, CA, United States of America
*
Correspondence to: Professor J.I.E. Hoffman, BS Hons (Wits), MD (Wits), 925 Tiburon Boulevard, Tiburon, CA 94920-1525. Tel: 415-435-6941; Fax: 415-435-6941; E-mail: julien.hoffman@ucsf.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Severe cyanosis due to pulmonary arteriovenous fistulas occurs often after a bidirectional superior cavopulmonary anastomosis (Glenn operation) and also in some congenital anomalies in which hepatic venous blood bypasses the lungs in the first passage. Relocation of hepatic flow into the lungs usually causes these fistulas to disappear. Similar pulmonary arteriovenous fistulas are observed in hereditary haemorrhagic telangiectasia, and in liver disease (hepatopulmonary syndrome). There is no convincing identification yet of a responsible hepatic factor that produces these lesions. Candidates for such a factor are reviewed, and the possibility of angiotensin or bradykinin contributing to the fistulas is discussed.

Keywords

Cavopulmonary anastomosishepatopulmonary syndromeangiogenesishepatic venous flowpulmonary arteriovenous fistulas

Information

Type
Review Articles
Information
Cardiology in the Young , Volume 23 , Issue 5 , October 2013 , pp. 629 - 641
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

1. Rahn, H, Fenn, WO. A Graphical Analysis of the Respiratory Gas Exchange. American Physiological Society, Washington, DC, 1955.Google Scholar
2. Riley, RL, Cournand, A. Ideal alveolar air and the analysis of ventilation–perfusion relationships in the lungs. J Appl Physiol 1949; 1: 825–847.CrossRefGoogle ScholarPubMed
3. Vogiatzis, I, Zakynthinos, S, Boushel, R, et al. The contribution of intrapulmonary shunts to the alveolar-to-arterial oxygen difference during exercise is very small. J Physiol 2008; 586: 2381–2391.Google Scholar
4. Wagner, PD, Gale, GE, Moon, RE, Torre-Bueno, JR, Stolp, BW, Saltzman, HA. Pulmonary gas exchange in humans exercising at sea level and simulated altitude. J Appl Physiol 1986; 61: 260–270.Google Scholar
5. Hammond, MD, Gale, GE, Kapitan, KS, Ries, A, Wagner, PD. Pulmonary gas exchange in humans during exercise at sea level. J Appl Physiol 1986; 60: 1590–1598.Google Scholar
6. Davis, HH II, Schwartz, DJ, Lefrak, SS, Susman, N, Schainker, BA. Alveolar-capillary oxygen disequilibrium in hepatic cirrhosis. Chest 1978; 73: 507–511.CrossRefGoogle ScholarPubMed
7. Schraufnagel, DE, Kay, JM. Structural and pathologic changes in the lung vasculature in chronic liver disease. Clin Chest Med 1996; 17: 1–15.Google Scholar
8. Feinstein, JA, Moore, P, Rosenthal, DN, Puchalski, M, Brook, MM. Comparison of contrast echocardiography versus cardiac catheterization for detection of pulmonary arteriovenous malformations. Am J Cardiol 2002; 89: 281–285.Google Scholar
9. Larsson, ES, Solymar, L, Eriksson, BO, de Wahl Granelli, A, Mellander, M. Bubble contrast echocardiography in detecting pulmonary arteriovenous malformations after modified Fontan operations. Cardiol Young 2001; 11: 505–511.Google Scholar
10. Chang, RK, Alejos, JC, Atkinson, D, et al. Bubble contrast echocardiography in detecting pulmonary arteriovenous shunting in children with univentricular heart after cavopulmonary anastomosis. J Am Coll Cardiol 1999; 33: 2052–2058.CrossRefGoogle ScholarPubMed
11. Nelson, NM, Prod'Hom, LS, Cherry, RB, Lipsitz, PJ, Smith, CA. Pulmonary function in the newborn infant: the alveolar-arterial oxygen gradient. J Appl Physiol 1963; 18: 534–538.Google Scholar
12. Stickland, MK, Welsh, RC, Haykowsky, MJ, et al. Intra-pulmonary shunt and pulmonary gas exchange during exercise in humans. J Physiol 2004; 561: 321–329.Google Scholar
13. Eldridge, MW, Dempsey, JA, Haverkamp, HC, Lovering, AT, Hokanson, JS. Exercise-induced intrapulmonary arteriovenous shunting in healthy humans. J Appl Physiol 2004; 97: 797–805.Google Scholar
14. Kim, SJ, Bae, EJ, Cho, DJ, et al. Development of pulmonary arteriovenous fistulas after bidirectional cavopulmonary shunt. Ann Thorac Surg 2000; 70: 1918–1922.Google Scholar
15. McMullan, DM, Hanley, FL, Cohen, GA, Portman, MA, Riemer, RK. Pulmonary arteriovenous shunting in the normal fetal lung. J Am Coll Cardiol 2004; 44: 1497–1500.Google Scholar
16. Butler, BD, Hills, BA. The lung as a filter for microbubbles. J Appl Physiol 1979; 47: 537–543.Google Scholar
17. Whyte, MK, Peters, AM, Hughes, JM, et al. Quantification of right to left shunt at rest and during exercise in patients with pulmonary arteriovenous malformations. Thorax 1992; 47: 790–796.Google Scholar
18. Wolfe, JD, Tashkin, DP, Holly, FE, Brachman, MB, Genovesi, MG. Hypoxemia of cirrhosis: detection of abnormal small pulmonary vascular channels by a quantitative radionuclide method. Am J Med 1977; 63: 746–754.Google Scholar
19. Cloutier, A, Ash, JM, Smallhorn, JF, et al. Abnormal distribution of pulmonary blood flow after the Glenn shunt or Fontan procedure: risk of development of arteriovenous fistulae. Circulation 1985; 72: 471–479.Google Scholar
20. Vettukattil, JJ, Slavik, Z, Lamb, RK, et al. Intrapulmonary arteriovenous shunting may be a universal phenomenon in patients with the superior cavopulmonary anastomosis: a radionuclide study. Heart 2000; 83: 425–428.Google Scholar
21. Ring, GC, Blum, AS, Kurbatov, T, Moss, WG, Smith, W. Size of microspheres passing through pulmonary circuit in the dog. Am J Physiol 1961; 200: 1191–1196.CrossRefGoogle ScholarPubMed
22. Lovering, AT, Stickland, MK, Kelso, AJ, Eldridge, MW. Direct demonstration of 25- and 50-microm arteriovenous pathways in healthy human and baboon lungs. Am J Physiol Heart Circ Physiol 2007; 292: H1777–H1781.Google Scholar
23. Groniowski, J. Morphological investigations on pulmonary circulation in the neonatal period. Am J Dis Child 1960; 99: 516–523.Google Scholar
24. Elliott, FM, Reid, L. Some new facts about the pulmonary artery and its branching pattern. Clin Radiol 1965; 16: 193–198.Google Scholar
25. Tobin, CE. Arteriovenous shunts in the peropheral pulmonary circulation in the human lung. Thorax 1966; 21: 197–204.Google Scholar
26. Wilkinson, MJ, Fagan, DG. Postmortem demonstration of intrapulmonary arteriovenous shunting. Arch Dis Child 1990; 65: 435–437.Google Scholar
27. Short, AC, Montoya, ML, Gebb, SA, Presson, RG Jr, Wagner, WW Jr, Capen, RL. Pulmonary capillary diameters and recruitment characteristics in subpleural and interior networks. J Appl Physiol 1996; 80: 1568–1573.Google Scholar
28. Miura, A, Nakamura, K, Matsubara, H, et al. Differences of diameter of pulmonary capillary vessels in patients with pulmonary hypertension using scanning electron microscope. Circulation 2011; 122:Abstract 21460.Google Scholar
29. Lomas, DJ, Hayball, MP, Jones, DP, Sims, C, Allison, ME, Alexander, GJ. Non-invasive measurement of azygos venous blood flow using magnetic resonance. J Hepatol 1995; 22: 399–403.Google Scholar
30. Debatin, JF, Zahner, B, Meyenberger, C, et al. Azygos blood flow: phase contrast quantitation in volunteers and patients with portal hypertension pre- and postintrahepatic shunt placement. Hepatology 1996; 24: 1109–1115.Google Scholar
31. Bosch, J, Mastai, R, Kravetz, D, Bruix, J, Rigau, J, Rodes, J. Measurement of azygos venous blood flow in the evaluation of portal hypertension in patients with cirrhosis. Clinical and haemodynamic correlations in 100 patients. J Hepatol 1985; 1: 125–139.Google Scholar
32. Mathur, M, Glenn, WW. Long-term evaluation of cava-pulmonary artery anastomosis. Surgery 1973; 74: 899–916.Google Scholar
33. McFaul, RC, Tajik, AJ, Mair, DD, Danielson, GK, Seward, JB. Development of pulmonary arteriovenous shunt after superior vena cava-right pulmonary artery (Glenn) anastomosis. Report of four cases. Circulation 1977; 55: 212–216.CrossRefGoogle ScholarPubMed
34. Trusler, GA, Williams, WG, Cohen, AJ, et al. William Glenn lecture: the cavopulmonary shunt. Evolution of a concept. Circulation 1990; 82: IV131–IV138.Google Scholar
35. Kopf, GS, Laks, H, Stansel, HC, Hellenbrand, WE, Kleinman, CS, Talner, NS. Thirty-year follow-up of superior vena cava-pulmonary artery (Glenn) shunts. J Thorac Cardiovasc Surg 1990; 100: 662–670.CrossRefGoogle ScholarPubMed
36. Duncan, BW, Desai, S. Pulmonary arteriovenous malformations after cavopulmonary anastomosis. Ann Thorac Surg 2003; 76: 1759–1766.Google Scholar
37. Chuang, VP, Mena, CE, Hoskins, PA. Congenital anomalies of the inferior vena cava. Review of embryogenesis and presentation of a simplified classification. Br J Radiol 1974; 47: 206–213.Google Scholar
38. Mayo, J, Gray, R, St Louis, E, Grosman, H, McLoughlin, M, Wise, D. Anomalies of the inferior vena cava. Am J Roentgenol 1983; 140: 339–345.Google Scholar
39. Debich, DE, Devine, WA, Anderson, RH. Polysplenia with normally structured hearts. Am J Cardiol 1990; 65: 1274–1275.Google Scholar
40. Guardado, FJ, Byrd, TM, Petersen, WG. Azygous continuation of the inferior vena cava with anomalous hepatic vein drainage. Am J Med Sci 2012; 343: 259–261.Google Scholar
41. Celentano, C, Malinger, G, Rotmensch, S, Gerboni, S, Wolman, Y, Glezerman, M. Prenatal diagnosis of interrupted inferior vena cava as an isolated finding: a benign vascular malformation. Ultrasound Obstet Gynecol 1999; 14: 215–218.Google Scholar
42. Kawashima, Y, Kitamura, S, Matsuda, H, Shimazaki, Y, Nakano, S, Hirose, H. Total cavopulmonary shunt operation in complex cardiac anomalies. A new operation. J Thorac Cardiovasc Surg 1984; 87: 74–81.Google Scholar
43. Kawashima, Y, Matsuki, O, Yagihara, T, Matsuda, H. Total cavopulmonary shunt operation. Semin Thorac Cardiovasc Surg 1994; 6: 17–20.Google Scholar
44. Brown, JW, Ruzmetov, M, Vijay, P, Rodefeld, MD, Turrentine, MW. Pulmonary arteriovenous malformations in children after the Kawashima operation. Ann Thorac Surg 2005; 80: 1592–1596.Google Scholar
45. Kutty, S, Frommelt, MA, Danford, DA, Tweddell, JS. Medium-term outcomes of Kawashima and completion Fontan palliation in single-ventricle heart disease with heterotaxy and interrupted inferior vena cava. Ann Thorac Surg 2010; 90: 1609–1613.Google Scholar
46. Srivastava, D, Preminger, T, Lock, JE, et al. Hepatic venous blood and the development of pulmonary arteriovenous malformations in congenital heart disease. Circulation 1995; 92: 1217–1222.Google Scholar
47. Vollebregt, A, Pushparajah, K, Rizvi, M, et al. Outcomes following the Kawashima procedure for single-ventricle palliation in left atrial isomerism. Eur J Cardiothorac Surg 2012; 41: 574–579.Google Scholar
48. Setyapranata, S, Brizard, CP, Konstantinov, IE, Iyengar, A, Cheung, M, d'Udekem, Y. Should we always plan a Fontan completion after a Kawashima procedure? Eur J Cardiothorac Surg 2011; 40: 1011–1015.Google Scholar
49. Papagiannis, J, Kanter, RJ, Effman, EL, et al. Polysplenia with pulmonary arteriovenous malformations. Pediatr Cardiol 1993; 14: 127–129.Google Scholar
50. Gurses, D, Ulger, Z, Levent, E, Ozyurek, AR. A very rare case of polysplenia syndrome with congenital diffuse pulmonary arteriovenous fistulas. Turk J Pediatr 2006; 48: 96–99.Google Scholar
51. Kawata, H, Kishimoto, H, Ikawa, S, et al. Pulmonary and systemic arteriovenous fistulas in patients with left isomerism. Cardiol Young 1998; 8: 290–294.Google Scholar
52. Agnoletti, G, Borghi, A, Annecchino, FP, Crupi, G. Regression of pulmonary fistulas in congenital heart disease after redirection of hepatic venous flow to the lungs. Ann Thorac Surg 2001; 72: 909–911.Google Scholar
53. Lee, J, Menkis, AH, Rosenberg, HC. Reversal of pulmonary arteriovenous malformation after diversion of anomalous hepatic drainage. Ann Thorac Surg 1998; 65: 848–849.CrossRefGoogle ScholarPubMed
54. Brochard, P, Lejonc, JL, Loisance, DY, Nitenberg, A. A rare cause of cyanosis and polycythemia: anomalous systemic venous connections without associated intracardiac malformations. The blue milkman story. Eur Heart J 1981; 2: 227–233.Google Scholar
55. Kirsch, J, Araoz, PA, Breen, JF, Chareonthaitawee, P. Isolated total anomalous connection of the hepatic veins to the left atrium. J Cardiovasc Comput Tomogr 2007; 1: 55–57.Google Scholar
56. Kloppenburg, GT, Post, MC, Mager, HJ, Schepens, MA. Rerouting anomalous hepatic venous connection to the left atrium. Ann Thorac Surg 2010; 90: 638–640.Google Scholar
57. Stoller, JK, Hoffman, RM, White, RD, Mee, RB. Anomalous hepatic venous drainage into the left atrium: an unusual cause of hypoxemia. Respir Care 2003; 48: 58–62.Google Scholar
58. Al-Ammouri, I, Shomali, W, Alsmady, MM, et al. Anomalous inferior vena cava drainage to the left atrium with successful staged repair in a 32-year-old woman with arthritis. Pediatr Cardiol 2010; 31: 912–914.Google Scholar
59. Black, H, Smith, GT, Goodale, WT. Anomalous inferior vena cava draining into the left atrium associated with intact interatrial septum and multiple pulmonary arteriovenous fistulae. Circulation 1964; 29: 258–267.Google Scholar
60. Gardner, DL, Cole, L. Long survival with inferior vena cava draining into left atrium. Br Heart J 1955; 17: 93–97.Google Scholar
61. Sierig, G, Vondrys, D, Daehnert, I. Anomalous drainage of the inferior caval vein to the left atrium. Cardiol Young 2005; 15: 85–87.Google Scholar
62. Kogon, BE, Fyfe, D, Butler, H, Kanter, KR. Anomalous drainage of the inferior vena cava into the left atrium. Pediatr Cardiol 2006; 27: 183–185.Google Scholar
63. Meadows, WR, Bergstrand, I, Sharp, JT. Isolated anomalous connection of a great vein to the left atrium. The syndrome of cyanosis and clubbing, “normal” heart, and left ventricular hypertrophy on electrocardiogram. Circulation 1961; 24: 669–676.Google Scholar
64. Venables, AW. Isolated drainage of the inferior vena cava to the left atrium. Br Heart J 1963; 25: 545–548.Google Scholar
65. Bernstein, HS, Ursell, PC, Brook, MM, Hanley, FC, Silverman, NH, Bristow, J. Fulminant development of pulmonary arteriovenous fistulas in an infant after total cavopulmonary shunt. Pediatr Cardiol 1996; 17: 46–50.CrossRefGoogle Scholar
66. Duncan, BW, Kneebone, JM, Chi, EY, et al. A detailed histologic analysis of pulmonary arteriovenous malformations in children with cyanotic congenital heart disease. J Thorac Cardiovasc Surg 1999; 117: 931–938.CrossRefGoogle ScholarPubMed
67. Starnes, SL, Duncan, BW, Kneebone, JM, et al. Pulmonary microvessel density is a marker of angiogenesis in children after cavopulmonary anastomosis. J Thorac Cardiovasc Surg 2000; 120: 902–907.Google Scholar
68. Starnes, SL, Duncan, BW, Kneebone, JM, et al. Angiogenic proteins in the lungs of children after cavopulmonary anastomosis. J Thorac Cardiovasc Surg 2001; 122: 518–523.Google Scholar
69. Sloan, RD, Cooley, RN. Congenital pulmonary arteriovenous aneurysm. Am J Roentgenol Radium Ther Nucl Med 1953; 70: 183–210.Google Scholar
70. Rodriguez-Roisin, R, Krowka, MJ, Herve, P, Fallon, MB. Pulmonary-hepatic vascular disorders (PHD). Eur Respir J 2004; 24: 861–880.Google Scholar
71. Rodriguez-Roisin, R, Krowka, MJ. Hepatopulmonary syndrome – a liver-induced lung vascular disorder. New Engl J Med 2008; 358: 2378–2387.Google Scholar
72. Gupta, D, Vijaya, DR, Gupta, R, et al. Prevalence of hepatopulmonary syndrome in cirrhosis and extrahepatic portal venous obstruction. Am J Gastroenterol 2001; 96: 3395–3399.Google Scholar
73. Varghese, J, Ilias-basha, H, Dhanasekaran, R, Singh, S, Venkataraman, J. Hepatopulmonary syndrome – past to present. Ann Hepatol 2007; 6: 135–142.Google Scholar
74. 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.Google Scholar
75. Agusti, AG, Roca, J, Rodriguez-Roisin, R. Mechanisms of gas exchange impairment in patients with liver cirrhosis. Clin Chest Med 1996; 17: 49–66.Google Scholar
76. Herve, P, Lebrec, D, Brenot, F, et al. Pulmonary vascular disorders in portal hypertension. Eur Respir J 1998; 11: 1153–1166.Google Scholar
77. Thenappan, T, Goel, A, Marsboom, G, et al. A central role for CD68(+) macrophages in hepatopulmonary syndrome. Reversal by macrophage depletion. Am J Respir Crit Care Med 2011; 183: 1080–1091.Google Scholar
78. Zhang, ZJ, Yang, CQ. Progress in investigating the pathogenesis of hepatopulmonary syndrome. Hepatobiliary Pancreat Dis Int 2010; 9: 355–360.Google Scholar
79. De, BK, Sen, S, Biswas, PK, et al. Occurrence of hepatopulmonary syndrome in Budd–Chiari syndrome and the role of venous decompression. Gastroenterology 2002; 122: 897–903.Google Scholar
80. 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.Google Scholar
81. Howard, ER, Davenport, M. Congenital extrahepatic portocaval shunts – the Abernethy malformation. J Pediatr Surg 1997; 32: 494–497.Google Scholar
82. Knight, WB, Mee, RB. A cure for pulmonary arteriovenous fistulas? Ann Thorac Surg 1995; 59: 999–1001.CrossRefGoogle ScholarPubMed
83. Kwon, BS, Bae, EJ, Kim, GB, Noh, CI, Choi, JY, Yun, YS. Development of bilateral diffuse pulmonary arteriovenous fistula after Fontan procedure: is there nonhepatic factor? Ann Thorac Surg 2009; 88: 677–680.Google Scholar
84. Moore, JW, Kirby, WC, Madden, WA, Gaither, NS. Development of pulmonary arteriovenous malformations after modified Fontan operations. J Thorac Cardiovasc Surg 1989; 98: 1045–1050.Google Scholar
85. Justino, H, Benson, LN, Freedom, RM. Development of unilateral pulmonary arteriovenous malformations due to unequal distribution of hepatic venous flow. Circulation 2001; 103: E39–E40.Google Scholar
86. McElhinney, DB, Marx, GR, Marshall, AC, Mayer, JE, Del Nido, PJ. Cavopulmonary pathway modification in patients with heterotaxy and newly diagnosed or persistent pulmonary arteriovenous malformations after a modified Fontan operation. J Thorac Cardiovasc Surg 2011; 141: 1362–1370; e1361.Google Scholar
87. Nakamura, Y, Yagihara, T, Kagisaki, K, Hagino, I, Kobayashi, J. Pulmonary arteriovenous malformations after a Fontan operation in the left isomerism and absent inferior vena cava. Eur J Cardiothorac Surg 2009; 36: 69–76.Google Scholar
88. Pike, NA, Vricella, LA, Feinstein, JA, Black, MD, Reitz, BA. Regression of severe pulmonary arteriovenous malformations after Fontan revision and “hepatic factor” rerouting. Ann Thorac Surg 2004; 78: 697–699.Google Scholar
89. Nakata, T, Fujimoto, Y, Hirose, K, et al. Fontan completion in patients with atrial isomerism and separate hepatic venous drainage. Eur J Cardiothorac Surg 2010; 37: 1264–1270.Google Scholar
90. Aidala, E, Chiappa, E, Cascarano, MT, Valori, A, Abbruzzese, PA. Partial hepatic vein diversion in pulmonary arteriovenous malformations in congenital heart disease. Ann Thorac Surg 2004; 78: 1089–1090.Google Scholar
91. Baskett, RJ, Ross, DB, Warren, AE, Sharratt, GP, Murphy, DA. Hepatic vein to the azygous vein anastomosis for pulmonary arteriovenous fistulae. Ann Thorac Surg 1999; 68: 232–233.Google Scholar
92. Ichikawa, H, Fukushima, N, Ono, M, et al. Resolution of pulmonary arteriovenous fistula by redirection of hepatic venous blood. Ann Thorac Surg 2004; 77: 1825–1827.Google Scholar
93. Kim, SJ, Bae, EJ, Lee, JY, Lim, HG, Lee, C, Lee, CH. Inclusion of hepatic venous drainage in patients with pulmonary arteriovenous fistulas. Ann Thorac Surg 2009; 87: 548–553.CrossRefGoogle ScholarPubMed
94. Lopez Enriquez, E, Martinez Catinchi, F, Johnson, C. Pulmonary arteriovenous fistula: report of a case. Bol Asoc Med P R 1976; 68: 217–220.Google Scholar
95. McElhinney, DB, Kreutzer, J, Lang, P, Mayer, JE Jr, del Nido, PJ, Lock, JE. Incorporation of the hepatic veins into the cavopulmonary circulation in patients with heterotaxy and pulmonary arteriovenous malformations after a Kawashima procedure. Ann Thorac Surg 2005; 80: 1597–1603.Google Scholar
96. Steinberg, J, Alfieris, GM, Brandt, B III, et al. New approach to the surgical management of pulmonary arteriovenous malformations after cavopulmonary anastomosis. Ann Thorac Surg 2003; 75: 1640–1642.Google Scholar
97. Wu, IH, Nguyen, KH. Redirection of hepatic drainage for treatment of pulmonary arteriovenous malformations following the Fontan procedure. Pediatr Cardiol 2006; 27: 519–522.Google Scholar
98. Shah, MJ, Rychik, J, Fogel, MA, Murphy, JD, Jacobs, ML. Pulmonary AV malformations after superior cavopulmonary connection: resolution after inclusion of hepatic veins in the pulmonary circulation. Ann Thorac Surg 1997; 63: 960–963.Google Scholar
99. Burstein, DS, Mavroudis, C, Puchalski, MD, Stewart, RD, Blanco, CJ, Jacobs, ML. Pulmonary arteriovenous malformations in heterotaxy syndrome: the case for early, direct hepatic vein-to-azygos vein connection. World J Pediatr Cong Heart Surg 2011; 2: 119–128.Google Scholar
100. Georghiou, GP, Erez, E, Bruckheimer, E, Dagan, O, Vidne, BA, Birk, E. Anomalous hepatic venous drainage. Ann Thorac Surg 2005; 80: 1113–1115.Google Scholar
101. Bradley, SE, Ingelfinger, FJ, et al. The estimation of hepatic blood flow in man. J Clin Invest 1945; 24: 890–897.Google Scholar
102. Wiklund, L. Human hepatic blood flow and its relation to systemic circulation during intravenous infusion of bupivacaine or etidocaine. Acta Anaesthesiol Scand 1977; 21: 189–199.Google Scholar
103. McAllister, KA, Grogg, KM, Johnson, DW, et al. Endoglin, a TGF-beta binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat Genet 1994; 8: 345–351.Google Scholar
104. McAllister, KA, Lennon, F, Bowles-Biesecker, B, et al. Genetic heterogeneity in hereditary haemorrhagic telangiectasia: possible correlation with clinical phenotype. J Med Genet 1994; 31: 927–932.Google Scholar
105. Berg, JN, Gallione, CJ, Stenzel, TT, et al. The activin receptor-like kinase 1 gene: genomic structure and mutations in hereditary hemorrhagic telangiectasia type 2. Am J Hum Genet 1997; 61: 60–67.Google Scholar
106. van den Driesche, S, Mummery, CL, Westermann, CJ. Hereditary hemorrhagic telangiectasia: an update on transforming growth factor beta signaling in vasculogenesis and angiogenesis. Cardiovasc Res 2003; 58: 20–31.Google Scholar
107. Lebrin, F, Goumans, MJ, Jonker, L, et al. Endoglin promotes endothelial cell proliferation and TGF-beta/ALK1 signal transduction. Embo J 2004; 23: 4018–4028.Google Scholar
108. David, L, Mallet, C, Keramidas, M, et al. Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ Res 2008; 102: 914–922.Google Scholar
109. Schwarte-Waldhoff, I, Schmiegel, W. Smad4 transcriptional pathways and angiogenesis. Int J Gastrointest Cancer 2002; 31: 47–59.Google Scholar
110. Nyberg, P, Xie, L, Kalluri, R. Endogenous inhibitors of angiogenesis. Cancer Res 2005; 65: 3967–3979.Google Scholar
111. Ribatti, D. Endogenous inhibitors of angiogenesis: a historical review. Leuk Res 2009; 33: 638–644.Google Scholar
112. Baghdady, Y, Hussein, Y, Shehata, M. Vascular endothelial growth factor in children with cyanotic and acyanotic and congenital heart disease. Arch Med Sci 2010; 6: 221–225.Google Scholar
113. El-Melegy, NT, Mohamed, NA. Angiogenic biomarkers in children with congenital heart disease: possible implications. It J Pediatr 2010; 36: 32.Google Scholar
114. Aydin, HI, Yozgat, Y, Demirkaya, E, et al. Correlation between vascular endothelial growth factor and leptin in children with cyanotic congenital heart disease. Turk J Pediatr 2007; 49: 360–364.Google Scholar
115. Himeno, W, Akagi, T, Furui, J, et al. Increased angiogenic growth factor in cyanotic congenital heart disease. Pediatr Cardiol 2003; 24: 127–132.Google Scholar
116. Ootaki, Y, Yamaguchi, M, Yoshimura, N, Oka, S, Yoshida, M, Hasegawa, T. Vascular endothelial growth factor in children with congenital heart disease. Ann Thorac Surg 2003; 75: 1523–1526.Google Scholar
117. Starnes, SL, Duncan, BW, Kneebone, JM, et al. Vascular endothelial growth factor and basic fibroblast growth factor in children with cyanotic congenital heart disease. J Thorac Cardiovasc Surg 2000; 119: 534–539.Google Scholar
118. Suda, K, Matsumura, M, Miyanish, S, Uehara, K, Sugita, T, Matsumoto, M. Increased vascular endothelial growth factor in patients with cyanotic congenital heart diseases may not be normalized after a Fontan type operation. Ann Thorac Surg 2004; 78: 942–946; discussion 946–947.Google Scholar
119. Seppinen, L, Pihlajaniemi, T. The multiple functions of collagen XVIII in development and disease. Matrix Biol 2011; 30: 83–92.Google Scholar
120. Zheng, MJ. Endostatin derivative angiogenesis inhibitors. Chin Med J 2009; 122: 1947–1951.Google Scholar
121. Clement, B, Musso, O, Lietard, J, Theret, N. Homeostatic control of angiogenesis: a newly identified function of the liver? Hepatology 1999; 29: 621–623.Google Scholar
122. Musso, O, Theret, N, Heljasvaara, R, et al. Tumor hepatocytes and basement membrane-producing cells specifically express two different forms of the endostatin precursor, collagen XVIII, in human liver cancers. Hepatology 2001; 33: 868–876.Google Scholar
123. Teodoro, JG, Parker, AE, Zhu, X, Green, MR. p53-Mediated inhibition of angiogenesis through up-regulation of a collagen prolyl hydroxylase. Science 2006; 313: 968–971.Google Scholar
124. Lee, TY, Tjin Tham Sjin, RM, Movahedi, S, et al. Linking antibody Fc domain to endostatin significantly improves endostatin half-life and efficacy. Clin Cancer Res 2008; 14: 1487–1493.Google Scholar
125. Folkman, J. Antiangiogenesis in cancer therapy – endostatin and its mechanisms of action. Exp Cell Res 2006; 312: 594–607.Google Scholar
126. Herbst, RS, Hess, KR, Tran, HT, et al. Phase I study of recombinant human endostatin in patients with advanced solid tumors. J Clin Oncol 2002; 20: 3792–3803.Google Scholar
127. Thomas, JP, Arzoomanian, RZ, Alberti, D, et al. Phase I pharmacokinetic and pharmacodynamic study of recombinant human endostatin in patients with advanced solid tumors. J Clin Oncol 2003; 21: 223–231.Google Scholar
128. Field-Ridley, A, Heljasvara, R, Pihlajaniemi, T, et al. Endostatin, an inhibitor of angiogenesis, decreases after bidirectional superior vena cava anastomosis. Pediatr Cardiol 2012; doi:10.1007/S00246-012-0441-2Google Scholar
129. Damico, R, Simms, T, Kim, BS, et al. p53 mediates cigarette smoke-induced apoptosis of pulmonary endothelial cells: inhibitory effects of macrophage migration inhibitor factor. Am J Respir Cell Mol Biol 2011; 44: 323–332.Google Scholar
130. Tipps, RS, Mumtaz, M, Leahy, P, Duncan, BW. Gene array analysis of a rat model of pulmonary arteriovenous malformations after superior cavopulmonary anastomosis. J Thorac Cardiovasc Surg 2008; 136: 283–289.Google Scholar
131. Brauer, R, Beck, IM, Roderfeld, M, Roeb, E, Sedlacek, R. Matrix metalloproteinase-19 inhibits growth of endothelial cells by generating angiostatin-like fragments from plasminogen. BMC Biochem 2011; 12: 38.Google Scholar
132. Gonzalez-Gronow, M, Grenett, HE, Fuller, GM, Pizzo, SV. The role of carbohydrate in the function of human plasminogen: comparison of the protein obtained from molecular cloning and expression in Escherichia coli and COS cells. Biochim Biophys Acta 1990; 1039: 269–276.Google Scholar
133. Fujiyama, S, Matsubara, H, Nozawa, Y, et al. Angiotensin AT(1) and AT(2) receptors differentially regulate angiopoietin-2 and vascular endothelial growth factor expression and angiogenesis by modulating heparin binding-epidermal growth factor (EGF)-mediated EGF receptor transactivation. Circ Res 2001; 88: 22–29.Google Scholar
134. Walther, T, Menrad, A, Orzechowski, HD, Siemeister, G, Paul, M, Schirner, M. Differential regulation of in vivo angiogenesis by angiotensin II receptors. FASEB J 2003; 17: 2061–2067.Google Scholar
135. de Resende, MM, Stodola, TJ, Greene, AS. Role of the renin angiotensin system on bone marrow-derived stem cell function and its impact on skeletal muscle angiogenesis. Physiol Genomics 2010; 42: 437–444.Google Scholar
136. Yin, T, Ma, X, Zhao, L, Cheng, K, Wang, H. Angiotensin II promotes NO production, inhibits apoptosis and enhances adhesion potential of bone marrow-derived endothelial progenitor cells. Cell Res 2008; 18: 792–799.Google Scholar
137. Grace, JA, Herath, CB, Mak, KY, Burrell, LM, Angus, PW. Update on new aspects of the renin–angiotensin system in liver disease: clinical implications and new therapeutic options. Clin Sci (Lond) 2012; 123: 225–239.Google Scholar
138. Clapp, C, Thebault, S, Jeziorski, MC, Martinez De La Escalera, G. Peptide hormone regulation of angiogenesis. Physiol Rev 2009; 89: 1177–1215.Google Scholar
139. Al-Merani, SA, Brooks, DP, Chapman, BJ, Munday, KA. The half-lives of angiotensin II, angiotensin II-amide, angiotensin III, Sar1-Ala8-angiotensin II and renin in the circulatory system of the rat. J Physiol 1978; 278: 471–490.Google Scholar
140. Bailie, MD, Rector, FC Jr, Seldin, DW. Angiotensin II in arterial and renal venous plasma and renal lymph in the dog. J Clin Invest 1971; 50: 119–126.Google Scholar
141. Semple, PF, Cumming, AM, Millar, JA. Angiotensins I and II in renal vein blood. Kidney Int 1979; 15: 276–282.Google Scholar
142. Admiraal, PJ, Danser, AH, Jong, MS, Pieterman, H, Derkx, FH, Schalekamp, MA. Regional angiotensin II production in essential hypertension and renal artery stenosis. Hypertension 1993; 21: 173–184.Google Scholar
143. Marshall, B, Duncan, BW, Jonas, RA. The role of angiogenesis in the development of pulmonary arteriovenous malformations in children after cavopulmonary anastomosis. Cardiol Young 1997; 7: 370–374.Google Scholar
144. Amaral, SL, Linderman, JR, Morse, MM, Greene, AS. Angiogenesis induced by electrical stimulation is mediated by angiotensin II and VEGF. Microcirculation 2001; 8: 57–67.Google Scholar
145. Amaral, SL, Papanek, PE, Greene, AS. Angiotensin II and VEGF are involved in angiogenesis induced by short-term exercise training. Am J Physiol Heart Circ Physiol 2001; 281: H1163–H1169.Google Scholar
146. Gwathmey, TM, Alzayadneh, EM, Pendergrass, KD, Chappell, MC. Novel roles of nuclear angiotensin receptors and signaling mechanisms. Am J Physiol Regul Integr Comp Physiol 2012; 302: R518–R530.Google Scholar
147. Gwathmey, TM, Westwood, BM, Pirro, NT, et al. Nuclear angiotensin-(1-7) receptor is functionally coupled to the formation of nitric oxide. Am J Physiol Renal Physiol 2010; 299: F983–F990.Google Scholar
148. Malhotra, SP, Reddy, VM, Thelitz, S, et al. Cavopulmonary anastomosis induces pulmonary expression of the angiotensin II receptor family. J Thorac Cardiovasc Surg 2002; 123: 655–660.Google Scholar
149. Malhotra, SP, Riemer, RK, Thelitz, S, He, YP, Hanley, FL, Reddy, VM. Superior cavopulmonary anastomosis suppresses the activity and expression of pulmonary angiotensin-converting enzyme. J Thorac Cardiovasc Surg 2001; 122: 464–469.Google Scholar
150. Gupta, LB, Kumar, A, Jaiswal, AK, et al. Pentoxifylline therapy for hepatopulmonary syndrome: a pilot study. Arch Int Med 2008; 168: 1820–1823.Google Scholar
151. Zhang, J, Ling, Y, Tang, L, et al. Pentoxifylline attenuation of experimental hepatopulmonary syndrome. J Appl Physiol 2007; 102: 949–955.CrossRefGoogle ScholarPubMed
152. Lumsden, AB, Henderson, JM, Kutner, MH. Endotoxin levels measured by a chromogenic assay in portal, hepatic and peripheral venous blood in patients with cirrhosis. Hepatology 1988; 8: 232–236.Google Scholar
153. Pidgeon, GP, Harmey, JH, Kay, E, Da Costa, M, Redmond, HP, Bouchier-Hayes, DJ. The role of endotoxin/lipopolysaccharide in surgically induced tumour growth in a murine model of metastatic disease. Br J Cancer 1999; 81: 1311–1317.Google Scholar