Plexiform Lesions in the Lungs of Domestic Fowl Selected for Susceptibility to Pulmonary Arterial Hypertension: Incidence and Histology

Anatomical Record

Volumn 294, Issue 5, 2011, Pages 739-755

  Wideman, Robert F ^a   Hamal, Krishna R ^a   Bayona, Michael T ^a   Lorenzoni, Alberto G ^a   Cross, David ^a   Khajali, Fariborz ^b   Rhoads, Douglas D ^a   Erf, Gisela F ^a   Anthony, Nicholas B ^a  

^a UNIVERSITY OF ARKANSAS   (United States)

^b SHAHREKORD UNIVERSITY   (Iran)

Author keywords

Chicken; Domestic fowl; Plexiform lesions; Pulmonary arterial hypertension; Pulmonary vasculature

Indexed keywords

AGE DISTRIBUTION; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY INTIMA PROLIFERATION; ARTICLE; CAGE; CELL INFILTRATION; CHICKEN; DISEASE PREDISPOSITION; DOMESTIC ANIMAL; FEMALE; HISTOLOGY; INCIDENCE; INFLAMMATION; MALE; MONONUCLEAR CELL; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PULMONARY ARTERY; PULMONARY ARTERY OCCLUSION; PULMONARY ARTERY PLEXIFORM LESION; PULMONARY HYPERTENSION; PULMONARY VASCULAR DISEASE; SEX DIFFERENCE;

ANIMALS; DISEASE SUSCEPTIBILITY; ENDOTHELIUM, VASCULAR; FEMALE; HYPERTENSION, PULMONARY; INCIDENCE; LUNG; MALE; POULTRY; POULTRY DISEASES; PULMONARY ARTERY;

ANIMALIA; GALLUS GALLUS;

EID: 79955878203     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.21369     Document Type: Article

References (152)

1. Abdalla MA, King AS. 1975. The functional anatomy of the pulmonary circulation of the domestic fowl. Respir Physiol 23: 267-290.
2. Abenhaim L, Moride Y, Brenot F, Rich S, Benichou J, Kurz X, Higenbottam T, Oakley C, Wouters E, Aubier M, Simonneau G, Begaud B. 1996. Appetite-suppressant drugs and the risk of primary pulmonary hypertension. N Engl J Med 335: 609-616.
3. Aird WC. 2003. Endothelial cell heterogeneity. Crit Care Med 31: S221-S230.
4. Albada ME, Schoemaker RG, Kemna MS, Cromme-Dijkhuis AH, van Veghel R, Berger RMF. 2005. The role of increased pulmonary blood flow in pulmonary hypertension. Eur Respir J 26: 487-493.
5. Anthony NB, Balog JM, Hughes JD, Stamps L, Cooper MA, Kidd BD, Liu X, Huff GR, Huff WE, Rath NC. 2001. Genetic selection of broiler lines that differ in their ascites susceptibility 1. Selection under hypobaric conditions. Proceedings 13th European Symposium on Poultry Nutrition, Blankenberge, Belgium, pp 327-328.
6. Archer S, Rich S. 2000. Primary pulmonary hypertension: a vascular biology and translational "work in progress." Circulation 102: 2781-2791.
7. 2-sensitive K+ channels in resistance pulmonary arteries explain regional heterogeneity in hypoxic pulmonary vasoconstriction: Ionic diversity in smooth muscle cells. Circ Res 95: 308-318.
8. Balog JM. 2003. Ascites syndrome (pulmonary hypertension syndrome) in broiler chickens: are we seeing the light at the end of the tunnel? Avian Poult Biol Rev 14: 99-126.
9. Barst RJ. 1986. Pharmacologically induced pulmonary vasodilation in children and young adults with primary pulmonary hypertension. Chest 89: 497-503.
10. Barst RJ, Loyd JE. 1998. Genetics and immunogenetic aspects of primary pulmonary hypertension. Chest 114: 231S-236S.
11. Berger RM, Geiger R, Hess J, Bogers AJJC, Mooi WI. 2001. Altered arterial expression patterns of inducible and endothelial nitric oxide synthase in pulmonary plexogenic arteriopathy caused by congenital heart disease. Am J Respir Crit Care Med 163: 1493-1499.
12. Botney MD. 1999. Role of hemodynamics in pulmonary vascular remodeling. Am J Respir Crit Care Med 159: 361-364.
13. Bottje WB, Wang S, Kelly FJ, Dunster C, Williams A, Mudway I. 1998. Antioxidant defenses in lung lining fluid of broilers: impact of poor ventilation conditions. Poult Sci 77: 516-522.
14. Bowen OT, Erf GF, Anthony NB, Wideman RF. 2006a. Pulmonary hypertension triggered by lipopolysaccharide (LPS) in ascites-susceptible and -resistant broilers is not amplified by aminoguanidine, a specific inhibitor of inducible nitric oxide synthase (iNOS). Poult Sci 85: 528-536.
15. Bowen OT, Wideman RF, Anthony NB, Erf GF. 2006b. Variation in the pulmonary hypertensive responsiveness of broilers to lipopolysaccharide (LPS) and innate variation in nitric oxide (NO) production by mononuclear cells? Poult Sci 85: 1349-1363.
16. Brenot F, Hervé P, Petitpretz P. 1993a. Primary pulmonary hypertension and the appetite suppressant fenfluramine. Br Heart J 89: 117-120.
17. Brenot F, Hervé P, Petitpretz P, Parent F, Duroux P, Simmoneu G. 1993b. Primary pulmonary hypertension and fenfluramine use. Br Heart J 70: 537-41.
18. Budhiraja R, Tuder RM, Hassoun PM. 2004. Endothelial dysfunction in pulmonary hypertension. Circulation 109: 159-165.
19. Caslin AW, Heath D, Madden B, Yacoub M, Gosney JR, Smith P. 1990. The histopathology of 36 cases of plexogenic pulmonary arteriopathy. Histopathology 16: 9-19.
20. Chapman ME, Wideman RF. 2001. Pulmonary wedge pressures confirm pulmonary hypertension in broilers is initiated by an excessive pulmonary arterial (Precapillary) resistance. Poult Sci 80: 468-73.
21. Chapman ME, Wideman RF. 2002. Hemodynamic responses of broiler pulmonary vasculature to intravenously infused serotonin. Poult Sci 81: 231-238.
22. Chapman ME, Wideman RF. 2006a. Evaluation of the serotonin receptor blockers ketanserin and methiothepin on the pulmonary hypertensive responses of broilers to intravenously infused serotonin. Poult Sci 85: 777-786.
23. Chapman ME, Wideman RF. 2006b. Evaluation of the serotonin receptor blocker Methiothepin in broilers injected intravenously with lipopolysaccharide and microparticles. Poult Sci 85: 2222-2230.
24. Chapman ME, Taylor RL, Jr, Wideman RF. 2008. Analysis of plasma serotonin levels and hemodynamic responses following chronic serotonin infusion in broilers challenged with bacterial lipopolysaccharide and microparticles. Poult Sci 87: 116-124.
25. Chazova I, Loyd JE, Zhdanov VS, Newman JH, Belenkov Y, Meyrick B. 1995. Pulmonary artery adventitial changes and venous involvement in primary pulmonary hypertension. Am J Pathol 146: 389-397.
26. Cisar CR, Balog JM, Anthony NB, Donoghue AM. 2003a. Sequence analysis of bone morphogenetic protein receptor type II mRNA from ascitic and nonascitic commercial broilers. Poult Sci 82: 1494-1499.
27. Cisar CR, Balog JM, Okimoto R, Anthony NB, Donoghue AM. 2003b. The chicken bone morphogenetic protein receptor type II (BMPR2) gene maps to chromosome 7. Anim Genet 34: 475-476.
28. Cool CD, Groshong SD, Oakey J, Voelkel NF. 2005. Pulmonary hypertension: cellular and molecular mechanisms. Chest 128: 565-571.
29. Cool CD, Kennedy D, Voelkel NF, Tuder RM. 1997. Pathogenesis and evolution of plexiform lesions in pulmonary hypertension associated with scleroderma and human immunodeficiency virus infection. Human Pathol 28: 434-442.
30. Cool CD, Stewart JS, Werahera P, Miller GJ, Williams RL, Voelkel NF, Tuder RM. 1999. Three-dimensional reconstruction of pulmonary arteries in plexiform pulmonary hypertension using cell-specific markers. Evidence for a dynamic and heterogeneous process of endothelial cell growth. Am J Pathol 155: 411-419.
31. Cueva S, Sillau H, Valenzuela A, Ploog H. 1974. High altitude induced pulmonary hypertension and right ventricular failure in broiler chickens. Res Vet Sci 16: 370-374.
32. Dammann JF, McEachen JA, Thompson WM, Smith R, Muller WH. 1961. The regression of pulmonary vascular disease after the creation of pulmonary stenosis. J Thoracic Cardiovasc Surg 42: 722-731.
33. Dorfmüller P, Perros F, Balabanian K, Humbert M. 2003. Inflammation in pulmonary arterial hypertension. Eur Respir J 22: 358-363.
34. Dorfmüller P, Zarka V, Durand-Gasselin I, Monti G, Balabanian K, Garcia G, Capron F, Coulomb-Lherminé A, Marfaing-Koka A, Simonneau G, Emilie D, Humbert M. 2002. Chemokine RANTES in severe pulmonary arterial hypertension. Am J Respir Crit Care Med 165: 534-539.
35. Douglas JG, Munro JF, Kitchin AH, Muir AL, Proudfoot AT. 1981. Pulmonary hypertension and fenfluramine. Br Med J 283: 881-883.
36. Duncker HR. 1972. Structure of avian lungs. Respir Physiol 14: 44-63.
37. Eddahibi S, Adnot S. 2002. Anorexigen-induced pulmonary hypertension and the serotonin (5-HT) hypothesis: lessons for the future in pathogenesis. Respir Res 3: 9-13.
38. Eddahibi S, Adnot S. 2005. The serotonin pathway in pulmonary hypertension. Adv Pulm Hypertension 4: Spring 2005. Available at.
39. Enkvetchakul B, Beasley J, Bottje W. 1995. Pulmonary arteriole hypertrophy in broilers with pulmonary hypertension syndrome (ascites). Poult Sci 74: 1676-1682.
40. Farber HW, Loscalzo J. 1999. Prothrombic hypertension mechanisms in primary pulmonary hypertension. J Lab Clin Med 134: 561-566.
41. Fedde MR, Weigle GE, Wideman RF. 1998. Influence of feed deprivation on ventilation and gas exchange in broilers: relationship to pulmonary hypertension syndrome. Poul Sci 77: 1704-1710.
42. Fishman AP. 2000. Changing concepts of the pulmonary plexiform lesion. Physiol Res 49: 485-492.
43. Frid MG, Aldashev AA, Dempsey EC, Stenmark KR. 1997. Smooth muscle cells isolated from discrete compartments of the mature vessel media exhibit unique phenotypes and distinct growth capabilities. Circ Res 81: 940-952.
44. Gurtner HP. 1985. Aminorex and pulmonary hypertension. A review. Cor Vasa 27: 160-171.
45. Gust R, Schuster DP. 2001. Vascular remodeling in experimentally induced subacute canine pulmonary hypertension. Exp Lung Res 27: 1-12.
46. Hamal KR, Wideman R, Anthony N, Erf GF. 2008. Expression of inducible nitric oxide synthase in lungs of broiler chickens following intravenous cellulose microparticle injection. Poult Sci 87: 636-644.
47. Heath D, Edwards JE. 1958. The pathology of hypertensive pulmonary vascular disease. A description of six grades of structural changes in the pulmonary arteries with special reference to congenital cardiac defects. Circulation 18: 533-547.
48. Heath D, Smith P, Gosney J. 1988. Ultrastructure of early plexogenic pulmonary arteriopathy. Histopathology 12: 41-52.
49. Heath D, Smith P, Gosney J, Mulcahy D, Fox K, Yacoub M, Harris P. 1987. The pathology of the early and late stages of primary pulmonary hypertension. Br Heart J 58: 204-213.
50. Hernandez A. 1987. Hypoxic ascites in broilers: a review of several studies done in Colombia. Avian Dis 31: 171-183.
51. Hervé P, Launay JM, Scrobohaci ML, Brenot F, Simonneau G, Petitpretz P, Poubeau P, Cerrina J, Duroux P, Drouet L. 1995. Increased plasma serotonin in primary pulmonary hypertension. Am J Med 99: 249-254.
52. Hoeper MM, Mayer E, Simonneau G, Rubin LJ. 2006. Chronic thromboembolic pulmonary hypertension. Circulation 113: 2011-2020.
53. Huchzermeyer FW, DeRuyck AMC. 1986. Pulmonary hypertension syndrome associated with ascites in broilers. Vet Rec 119: 94.
54. Humbert M, Morrell NW, Archer SL, Stenmark KR, MacLean MR, Lang IM, Christman BW, Weir EK, Eickelberg O, Voelkel NF, Rabinovitch M. 2004. Cellular and molecular pathobiology of pulmonary arterial hypertension. J Am Coll Cardiol 43: 13S-24S.
55. Ivy DD, McMurtry IF, Colvin K, Imamura M, Oka M, Lee D-S, Gebb S, James PL. 2005. Development of occlusive neointimal lesions in distal pulmonary arteries of endothelin B receptor-deficient rats: a new model of severe pulmonary artery hypertension. Circulation 111: 2988-2996.
56. Jamison BM, Michel MD. 1995. Different distribution of plexiform lesions in primary and secondary pulmonary hypertension. Human Pathol 26: 987-993.
57. Jandel Scientific. 1994. SigmaStat® Statistical Software User's Manual. Jandel Scientific Software, San Rafael. CA.
58. Jones JH, Effmann EL, Schmidt-Nielsen K. 1985. Lung volume changes during respiration in ducks. Respir Physiol 59: 15-25.
59. Julian RJ. 1988. Pulmonary hypertension as a cause of right ventricular failure and ascites in broilers. Zootecnica International (November, #11): 58-62.
60. Julian RJ. 1989. Lung volume of meat-type chickens. Avian Dis. 33: 174-176.
61. Kelly JJ, Moore TM, Babal P, Diwan AH, Stephens T, Thompson WJ. 1998. Pulmonary microvascular and macrovascular endothelial cells: differential regulation of Ca2+ and permeability. Am J Physiol 274: L810-L819.
62. Kentera D, Susic D, Veljkovic V, Tukacovic G, Koko V. 1988. Pulmonary artery pressure in rats with hereditary platelet function defect. Respiration 54: 110-114.
63. King AS. 1979. Systema respiratorium. In: Baumel JJ, King AS, Lucas AM, Breazile JE, Evans HE, editors. Nomina Anatomica Avium, 1st ed. New York: Academic Press. p 227-265.
64. King AS, King DZ, Abdalla MA. 1978. The structure of the intrapulmonary vasculature of the domestic fowl. In: Piiper J, editor. Respiratory function in birds, adult and embryonic. New York, NY: Springer-Verlag. p 112-124.
65. Lawrie A, Spiekerkoetter E, Martinez EC, Ambartsumian N, Sheward WJ, MacLean MR, Harmar AJ, Schmidt A-M, Lukanidin E, Rabinovitch M. 2005. Interdependent serotonin transporter and receptor pathways regulate S100A4/Mts1, a gene associated with pulmonary vascular disease. Circ Res 97: 227-235.
66. Le Cras TD, Kim DH, Gebb S, Markham NE, Shannon JM, Tuder RM, Abman SH. 1999. Abnormal lung growth and the development of pulmonary hypertension in the Fawn-Hooded rat. Am J Physiol 277: L709-L718.
67. Lee S-D, Shroyer KR, Markham NE, Cool CD, Voelkel NF, Tuder RM. 1998. Monoclonal endothelial cell proliferation is present in primary but not secondary pulmonary hypertension. J Clin Invest 101: 927-934.
68. Lorenzoni AG, Anthony NB, Wideman RF. 2008. Transpulmonary pressure gradient verifies pulmonary hypertension is initiated by increased arterial resistance in broilers. Poult Sci 87: 125-132
69. Louis WJ. 1999. Primary pulmonary hypertension and anorectic drugs. N Engl J Med 340: 481-482.
70. Loyd JE, Newman JH. 1997. Familial primary pulmonary hypertension. In: Rubin LJ, Rich S, editors. Primary pulmonary hypertension. New York, NY: Marcel Dekker, Inc. p 151-162.
71. Maina JN. 1988. Scanning electron microscope study of the spatial organization of the air and blood conducting components of the avian lung (Gallus gallus variant domesticus). Anat Rec 222: 145-153.
72. Marcos E, Fadel E, Sanchez O, Humbert M, Dartevelle P, Simonneau G, Hamon M, Adnot S, Eddahibi S. 2004. Serotonin-induced smooth muscle hyperplasia in various forms of human pulmonary hypertension. Circ Res 94: 1263-1270.
73. Mark EJ, Patalas ED, Chang HT, Evans RJ, Kessler SC. 1997. Fatal pulmonary hypertension associated with short-term use of fenfluramine and phentermine. New Engl J Med 337: 602-620.
74. Maxwell MH. 1991. Red cell size and various lung arterial measurements in different strains of domestic fowl. Res Vet Sci 50: 233-239.
75. McLaughlin VV. 2002. Pulmonary arterial hypertension: current diagnosis and management. ACC Current J Rev 11: 17-21.
76. Mecham RP, Whitehouse LA, Wrenn DS, Parks WC, Griffin GL, Senior RM, Crouch EC, Stenmark KR, Voelkel NF. 1987. Smooth muscle-mediated connective tissue remodeling in pulmonary hypertension. Science 237: 423-426.
77. Medhora M, Bousamra M, II, Zhu D, Somberg L, Jacobs ER. 2002. Upregulation of collagens detected by gene array in a model of flow-induced pulmonary vascular remodeling. Am J Physiol Heart Circ Physiol 282: H414-H422.
78. Meyrick B, Perkett EA, Brigham KL. 1987. Inflammation and models of chronic pulmonary hypertension. Am Rev Respir Dis 136: 765-767.
79. Moreno de Sandino M, Hernandez A. 2003. Nitric oxide synthase expression in the endothelium of pulmonary arterioles in normal and pulmonary hypertensive chickens subjected to chronic hypobaric hypoxia. Avian Dis 47: 1291-1297.
80. Moreno de Sandino M, Hernandez A. 2006. Pulmonary arteriole remodeling in hypoxic broilers expressing different amounts of endothelial nitric oxide synthase. Poult Sci 85: 899-901.
81. Morse JH. 2005. Defining the role and clinical relevance of BMPR2 mutations in pulmonary artery hypertension. Adv Pulm Hypertension 4:Spring 2005. Available at.
82. Naeije R, Eddahibi S. 2004. Serotonin in pulmonary arterial hypertension. Am J Respir Crit Care Med 70: 209-210.
83. Naeye RL, Vennart GP. 1959. The structure and significance of pulmonary plexiform structures. Am J Pathol 36: 593-605.
84. Nagaoka T, Gebb SA, Karoor V, Homma N, Morris KG, McMurtry IF, Oka M. 2006. Involvement of RhoA/Rho kinase signaling in pulmonary hypertension of the fawn-hooded rat. J Appl Physiol 100: 996-1002.
85. National Research Council. 1994. Nutrient Requirements of Poultry. 9th rev. ed. Washington, DC: National Academy Press.
86. Newman JH, Trembath RC, Morse JA, Grunig E, Loyd JE, Adnot S, Coccolo F, Ventura C, Phillips JA, Knowles JA, Janssen B, Eickelberg O, Eddahibi S, Herve P, Nichols WC, Elliot G. 2004. Genetic basis of pulmonary arterial hypertension. J Am Coll Cardiol 43: 33S-39S.
87. Nicolls MR, Taraseviciene-Stewart T, Rai PR, Badesch DB, Voelkel NF. 2005. Autoimmunity and pulmonary hypertension: a perspective. Eur Respir J 26: 1110-1118.
88. Nishimura T, Faul JL, Berry GJ, Vaszar LT, Qui D, Pearl RG, Kao PN. 2002. Simvastatin attenuates smooth muscle neointimal proliferation and pulmonary hypertension in rats. Am J Respir Crit Care Med 166: 1403-1408.
89. Nishimura T, Vaszar LT, Faul JL, Zhao G, Berry GM, Shi L, Qui D, Benson G, Pearl RG, Kao PN. 2003. Simvastatin rescues rats from fatal pulmonary hypertension by inducing apoptosis of neointimal smooth muscle cells. Circulation 108: 1640-1645.
90. Owen RL, Wideman RF, Barbato GF, Cowen BS, Ford BC, Hattel AL. 1995a. Morphometric and histologic changes in the pulmonary system of broilers raised at simulated high altitude. Avian Pathol 24: 293-302.
91. Owen RL, Wideman RF, Leach RM, Cowen BS, Dunn ZPA, Ford BC. 1995b. Physiologic and electrocardiographic changes occurring in broilers reared at simulated high altitude. Avian Dis 39: 108-115.
92. Palevsky HI, Schloo BL, Pietra GG, Weber KT, Janicki JS, Ruben E, Fishman AP. 1989. Primary pulmonary hypertension: vascular structure, morphometry and responsiveness to vasodilator agents. Circulation 80: 1207-1221.
93. Pan J-Q, Tan X, Li J-C, Sun W-D, Wang X-L. 2005. Effects of early feed restriction and cold temperature on lipid peroxidation, pulmonary vascular remodeling and ascites morbidity in broilers under normal and cold temperatures. Br Poult Sci 46: 374-381.
94. Pavlidis HO. 2003. Correlated responses of divergent selection for ascites in broilers. Master's Thesis. Dept. Poult. Sci. Univ. Arkansas, Fayetteville.
95. Pavlidis HO, Balog JM, Stamps LK, Hughes JD, Jr, Huff WE, Anthony NB. 2007. Divergent selection for ascites incidence in chickens. Poult Sci 86: 2517-2529.
96. Powell FL, Hastings RH, Mazzone RW. 1985. Pulmonary vascular resistance during unilateral pulmonary artery occlusion in ducks. Am J Physiol 249: R39-R43.
97. Peacock AJ, Picket C, Morris K, Reeves JT. 1989. The relationship between rapid growth and pulmonary hemodynamics in the fast-growing broiler chicken. Am Rev Respir Dis 139: 1524-1530.
98. Peacock AJ, Pickett C, Morris K, Reeves JT. 1990. Spontaneous hypoxaemia and right ventricular hypertrophy in fast growing broiler chickens reared at sea level. Comp Biochem Physiol 97A: 537-541.
99. Pietra GG. 1997. The pathology of primary pulmonary hypertension. In: Rubin LJ, Rich S, editors. Primary pulmonary hypertension: lung biology in health and disease. New York, NY: Marcel Dekker, Inc. p 19-61.
100. Pietra GG, Capron F, Stewart S, Leone O, Humbert M, Robbins IM, Reid LM, Tuder RM. 2004. Pathologic assessment of vasculopathies in pulmonary hypertension. J Am Coll Cardiol 43: 25S-32S.
101. Rabinovitch M. 1997. Insights into the pathogenesis of primary pulmonary hypertension from animal models. In: Rubin LJ, Rich S, editors. Primary pulmonary hypertension. New York, NY: Marcel Dekker, Inc. p 63-82.
102. Rabinovitch M, Keane JF, Norwood WI, Castaneda AR, Reid L. 1984. Vascular structure in lung tissue obtained at biopsy correlated with pulmonary hemodynamic findings after repair of congenital heart defects. Circulation 69: 655-667.
103. Rich S. 1998. Clinical insights into the pathogenesis of primary pulmonary hypertension. Chest 114: 237S-241S.
104. Richter A, Yeager ME, Zaiman A, Cool CD, Voelkel NF, Tuder RM. 2004. Impaired transforming growth factor-β signaling in idiopathic pulmonary arterial hypertension. Am J Respir Crit Care Med 170: 1340-1348.
105. Rubin LJ. 1997. Primary pulmonary hypertension. N Engl J Med 336: 111-117.
106. Sakao S, Taraseviciene-Stewart L, Lee JD, Wood K, Cool CD, Voelkel NF. 2005. Initial apoptosis is followed by increased proliferation of apoptosis-resistant endothelial cells. FASEB J 19: 1178-1180.
107. Saldana ME, Harley RA, Liebow AA, Carrington CB. 1968. Experimental extreme pulmonary hypertension and vascular disease in relation to polycythemia. Am J Pathol 52: 935-981.
108. Sato K, Webb S, Tucker A, Rabinovitch M, O'Brien RF, McMurtry IF, Stelzner TJ. 1992. Factors influencing the idiopathic development of pulmonary hypertension in the fawn hooded rat. Am Rev Respir Dis 145: 793-797.
109. Schnader SM, Schloo BL, Anderson W, Stephenson LW, Fishman AP. 1996. Chronic pulmonary hypertension in sheep: temporal progression of lesions. J Surg Res 62: 243-250.
110. Sillau AH, Montalvo C. 1982. Pulmonary hypertension and the smooth muscle of pulmonary arterioles in chickens at high altitude. Comp Biochem Physiol 71A: 125-130.
111. Silversides FG, LeFrancois MR, Villeneuve P. 1997. The effect of strain of broiler on physiological parameters associated with the ascites syndrome. Poult Sci 76: 663-667.
112. Simonneau G, Galie N, Rubin LJ, Langleben D, Seeger W, Domenighetti G, Gibbs S, Lebrec D, Speich R, Beghetti M, Rich S, Fishman A. 2004. Clinical classification of pulmonary hypertension. J Am Coll Cardiol 43: 5S-12S.
113. Stelzner TJ, O'Brien RF, Sato K, Webb S, Zamora MR, Sakurai T, Yanagisawa M, McMurtry IF, Fisher J. 1992. Increased endothelin-1 expression in rats with pulmonary hypertension. Am J Physiol 262: L614-L620.
114. Stevens T. 2005. Molecular and cellular determinants of lung endothelial cell heterogeneity. Chest 128: 558-564.
115. Stevens T, Rosenberg R, Aird W, Quertermous T, Johnson FJ, Garcia JGN, Hebbel RP, Tuder RM, Garfinkel S. 2001. NHLBI workshop report: endothelial cell phenotypes in heart, lung, and blood diseases. Am J Physiol Cell Physiol 281: C1422-C1433.
116. Tan X, Liu Y-J, Li J-C, Pan J-Q, Sun W-D, Wang X-L. 2005a. Activation of PCKα and pulmonary vascular remodeling in broilers. Res Vet Sci 79: 131-137.
117. Tan X, Pan J-Q, Li J-C, Liu Y-J, Sun W-D, Wang X-L. 2005b. L-Arginine inhibiting pulmonary vascular remodelling is associated with promotion of apoptosis in pulmonary arterioles smooth muscle cells in broilers. Res Vet Sci 79: 203-209.
118. Tanaka Y, Schuster DP, Davis EC, Patterson GA, Botney MD. 1996. The role of vascular injury and hemodynamics in rat pulmonary artery remodeling. J Clin Invest 98: 434-442.
119. Taraseviciene-Stewart L, Kasahara Y, Alger L, Hirth P, Mc Mahon GG, Waltenberger J, Voelkel NF, Tuder RM. 2001. Inhibition of the VEGF receptor 2 combined with chronic hypoxia causes cell death-dependent pulmonary endothelial cell proliferation and severe pulmonary hypertension. FASEB J 15: 427-438.
120. Taraseviciene-Stewart L, Scerbavicius R, Choe K-H, Cool C, Wood K, Tuder RM, Burns N, Kasper M, Voelkel NF. 2006. Simvastatin causes endothelial cell apoptosis and attenuates severe pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 291: L668-L676.
121. Tuder RM, Chacon M, Alger L, Wang J, Taraseviciene-Stewart L, Kasahara Y, Cool CD, Bishop AE, Geraci M, Semenza L, Yacoub M, Polak JM, Voelkel NF. 2001. Expression of angiogenesis-related molecules in plexiform lesions in severe pulmonary hypertension: evidence for a process of disordered angiogenesis. J Pathol 195: 367-374.
122. Tuder RM, Groves B, Badesch DB, Voelkel NF. 1994. Exuberant endothelial cell growth and elements of inflammation are present in plexiform lesions of pulmonary hypertension. Am J Pathol 144: 275-285.
123. Tuder RM, Lee S-D, Cool CC. 1998a. Histopathology of pulmonary hypertension. Chest 114: 1S-6S.
124. Tuder RM, Radisavljevic Z, Shroyer KR, Polak JM, Voelkel NF. 1998b. Monoclonal endothelial cells in appetite suppressant-associated pulmonary hypertension. Am J Respir Crit Care Med 158: 1999-2001.
125. Vaszar LT, Nishimura T, Storey JD, Zhao G, Qui D, Faul JL, Pearl RG, Kao PN. 2004. Longitudinal transcriptional analysis of developing neointimal vascular occlusion and pulmonary hypertension in rats. Physiol Genomics 17: 150-156.
126. Voelkel NF, Cool C, Lee SD, Wright L, Geraci MW, Tuder RM. 1998. Primary pulmonary hypertension between inflammation and cancer. Chest 114: 225S-230S.
127. Voelkel NF, Tuder RM, Weir EK. 1997. Pathophysiology of primary pulmonary hypertension: from physiology to molecular mechanisms. In: Rubin LJ, Rich S, editors. Primary pulmonary hypertension. New York, NY: Marcel Dekker, Inc. p 83-129.
128. Wagenvoort CA. 1980. Lung biopsy specimens in the evaluation of pulmonary vascular disease. Chest 77: 614-625.
129. Wagenvoort CA, Wagenvoort N. 1970. Primary pulmonary hypertension: a pathologic study of the lung vessels in 156 clinically diagnosed cases. Circulation 42: 1163-1184.
130. Wagenvoort CA, Wagenvoort N, Draulans-Noe Y. 1984. Reversibility of plexogenix pulmonary arteriopathy following banding of the pulmonary artery. J Thorac Cardiovasc Surg 87: 876-886.
131. Wang W, Erf GF, Wideman RF. 2002. Effect of cage vs. floor litter environments on the pulmonary hypertensive response to intravenous endotoxin and on blood-gas values in broilers. Poult Sci 81: 1728-1737.
132. Wang W, Wideman RF, Bersi TK, Erf GF. 2003. Pulmonary and hematological inflammatory responses to intravenous cellulose micro-particles in broilers. Poult Sci 82: 771-780.
133. Wideman RF. 1999. Cardiac Output in four-, five- and six-week-old broilers, and hemodynamic responses to intravenous injections of epinephrine. Poult Sci 78: 392-403.
134. Wideman RF. 2000. Cardio-pulmonary hemodynamics and ascites in broiler chickens. Avian and Poult Biol Rev 11:21-43.
135. Wideman RF. 2001. Pathophysiology of heart/lung disorders: pulmonary hypertension syndrome in broiler chickens. World's Poult Sci J 57: 289-307.
136. Wideman RF, Bowen OT, Erf GF, Chapman ME. 2006. Influence of aminoguanidine, an inhibitor of inducible nitric oxide synthase, on the pulmonary hypertensive response to micro-particle injections in broilers. Poult Sci 85: 511-527.
137. Wideman RF, Chapman ME, Hamal KR, Bowen OT, Lorenzoni AG, Erf GF, Anthony NB. 2007. An inadequate pulmonary vascular capacity and susceptibility to pulmonary arterial hypertension in broilers. Poult Sci 86: 984-998.
138. Wideman RF, Chapman ME, Owens CM, Devabhaktuni MK, Cavitt LC, Erf GF. 2003. Broiler survivors of intravenous micro-particle injections: evaluation of growth, livability, meat quality, and arterial blood gas values during a cyclic heat challenge. Poult Sci 82: 484-495.
139. Wideman RF, Erf GF. 2002. Intravenous micro-particle injections trigger pulmonary hypertension in broiler chickens. Poult Sci 81: 877-886.
140. Wideman RF, Erf GF, Chapman ME. 2005. Nω-Nitro-L-Arginine Methyl Ester (L-NAME) amplifies the pulmonary hypertensive response to micro-particle injections in broilers. Poult Sci 84: 1077-1091.
141. Wideman RF, Erf GF, Chapman ME, Wang W, Anthony NB, Xiaofong L. 2002. intravenous micro-particle injections and pulmonary hypertension in broiler chickens: acute post-injection mortality and ascites susceptibility. Poult Sci 81: 1203-1217.
142. Wideman RF, Kirby YK. 1995. Evidence of a ventilation-perfusion mismatch during acute unilateral pulmonary artery occlusion in broilers. Poult Sci 74: 1209-1217.
143. Wideman RF, Kirby YK, Tackett CD, Marson NE, McNew RW. 1996a. Cardio-pulmonary function during acute unilateral occlusion of the pulmonary artery in broilers fed diets containing normal or high levels of arginine-HCl. Poult Sci 75: 1587-1602.
144. Wideman RF, Kirby YK, Tackett CD, Marson NE, Tressler CJ, McNew RW. 1996b. Independent and simultaneous unilateral occlusion of the pulmonary artery and extra-pulmonary primary bronchus in broilers. Poult Sci 75: 1417-1427.
145. Wright L, Tuder RM, Wang J, Cool CD, Lepley RA, Voelkel NF. 1998. 5-Lipoxygenase and 5-lipoxygenase activating protein (FLAP) immunoreactivity in lungs from patients with primary pulmonary hypertension. Am J Respir Crit Care Med 157: 219-229.
146. Xiang RP, Sun WD, Wang JY, Wang XL. 2002. Effect of vitamin C on pulmonary hypertension and muscularization of pulmonary arterioles in broilers. Br Poult Sci 43: 705-712.
147. Xiang RP, Sun WD, Zhang KC, Li JC, Wang JY, Wang XL. 2004. Sodium chloride-induced acute and chronic pulmonary hypertension syndrome in broiler chickens. Poult Sci 83: 732-736.
148. Yaginuma G, Mohri H, Takahashi T. 1990. Distribution of arterial lesions and collateral pathways in the pulmonary hypertension of congenital heart disease: a computer aided reconstruction study. Thorax 45: 586-590.
149. Yamaki S, Wagenvoort CA. 1985. Comparison of primary plexogenic arteriopathy in adults and children. Br Heart J 54: 428-434.
150. Yi ES, Kim H, Ahn H, Strother J, Morris T, Masliah E, Hansen LA, Park K, Friedman PJ. 2000. Distribution of obstructive intimal lesions and their cellular phenotypes in chronic pulmonary hypertension. Am J Respir Crit Care Med 162: 1577-1586.
151. Zabka TS, Campbell FE, Wilson DW. 2006. Pulmonary arteriopathy and idiopathic pulmonary arterial hypertension in six dogs. Vet Pathol 43: 510-522.
152. Zamora MR, Stelzner TJ, Webb S, Panos RJ, Ruff LJ, Dempsey EC. 1996. Overexpression of endothelin-1 and enhanced growth of pulmonary artery smooth muscle cells from fawn-hooded rats. Am J Physiol 270: L101-L109.