Effects of vascular endothelial growth factor on survival of surgical flaps: A review of experimental studies

Journal of Reconstructive Microsurgery

Volumn 30, Issue 1, 2014, Pages 1-14

  Fang, Taolin ^a,b   Lineaweaver, William C ^c   Chen, Michael B ^a   Kisner, Carson ^a   Zhang, Feng ^a  

^a UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^b ZHONGSHAN HOSPITAL OF FUDAN UNIVERSITY   (China)

^c River Oaks Hospital   (United States)

Author keywords

flaps; mechanism; vascular endothelial growth factor

Indexed keywords

VASCULOTROPIN; VASCULOTROPIN RECEPTOR; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; VASCULOTROPIN RECEPTOR 3;

CAPILLARY DENSITY; CAPILLARY PERMEABILITY; ENDOTHELIAL PROGENITOR CELL; FLAP SURVIVAL; GENE THERAPY; GRACILIS MUSCLE; HUMAN; MODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SURGICAL FLAPS; SYSTEMATIC REVIEW; TISSUE SURVIVAL; VASODILATATION;

ANIMALS; GRAFT SURVIVAL; HUMANS; INTRAOPERATIVE PERIOD; PREOPERATIVE PERIOD; RECEPTORS, VASCULAR ENDOTHELIAL GROWTH FACTOR; SKIN TRANSPLANTATION; SURGICAL FLAPS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2; VASODILATION;

EID: 84891836382     PISSN: 0743684X     EISSN: 10988947     Source Type: Journal    
DOI: 10.1055/s-0033-1345429     Document Type: Review

References (126)

1. Sværdborg M., Birke-Sorensen H. Monitored extended secondary arterial ischemia in a free muscle transfer. J Reconstr Microsurg: 2012; 28 2 119 124
2. Kwee M. M., Rozen W. M., Ting J. WC, Mirkazemi M., Leong J., Baillieu C. Total scalp reconstruction with bilateral anterolateral thigh flaps. Microsurgery: 2012; 32 5 393 396
3. Kerrigan C. L., Stotland M. A. Ischemia reperfusion injury: a review. Microsurgery: 1993; 14 3 165 175
4. Carroll W. R., Esclamado R. M. Ischemia/reperfusion injury in microvascular surgery. Head Neck: 2000; 22 7 700 713
5. Pang C. Y. Ischemia-induced reperfusion injury in muscle flaps: pathogenesis and major source of free radicals. J Reconstr Microsurg: 1990; 6 1 77 83
6. Balasubramanian D., Thankappan K., Kuriakose M. A., et al. Reconstructive indications of simultaneous double free flaps in the head and neck: a case series and literature review. Microsurgery: 2012; 32 6 423 430
7. Haughey B. H., Panje W. R. Extension of the musculocutaneous flap by surgical delay. Arch Otolaryngol: 1985; 111 4 234 240
8. Taylor G. I., Corlett R. J., Caddy C. M., Zelt R. G. An anatomic review of the delay phenomenon: II. Clinical applications. Plast Reconstr Surg: 1992; 89 3 408 416, discussion 417-418
9. Attinger C. E., Picken C. A., Troost T. R., Sessions R. B. Minimizing pectoralis myocutaneous flap loss with the delay principle. Otolaryngol Head Neck Surg: 1996; 114 1 148 157
10. Grabb W., ed. Basic techniques of plastic surgery. Boston Little Brown: 1986
11. Huang N., Khan A., Ashrafpour H., et al. Efficacy and mechanism of adenovirus-mediated VEGF-165 gene therapy for augmentation of skin flap viability. Am J Physiol Heart Circ Physiol: 2006; 291 1 H127 H137
12. Knight K. R. Review of postoperative pharmacological infusions in ischemic skin flaps. Microsurgery: 1994; 15 10 675 684
13. Pang C. Y., Forrest C. R., Morris S. F. Pharmacological augmentation of skin flap viability: a hypothesis to mimic the surgical delay phenomenon or a wishful thought. Ann Plast Surg: 1989; 22 4 293 306
14. Waters L. M., Pearl R. M., Macaulay R. M. A comparative analysis of the ability of five classes of pharmacological agents to augment skin flap survival in various models and species: an attempt to standardize skin flap research. Ann Plast Surg: 1989; 23 2 117 122
15. Maeda M., Fukui A., Tamai S. Combined therapy with antithrombotic agents and radical scavengers for reperfusion injury of flaps. J Reconstr Microsurg: 1991; 7 3 233 243
16. Davis R. E., Wachholz J. H., Jassir D., Perlyn C. A., Agrama M. H. Comparison of topical anti-ischemic agents in the salvage of failing random-pattern skin flaps in rats. Arch Facial Plast Surg: 1999; 1 1 27 32
17. Forrest C. R., Pang C. Y., Zhong A. G., Kreidstein M. L. Efficacy of intravenous infusion of prostacyclin (PGI2) or prostaglandin E1 (PGE1) in augmentation of skin flap blood flow and viability in the pig. Prostaglandins: 1991; 41 6 537 558
18. Tuncer S., Ayhan S., Findikcioglu K., Ergun H., Tuncer I. Effect of systemic piracetam treatment on flap survival and vascular endothelial growth factor expression after ischemia-reperfusion injury. J Reconstr Microsurg: 2011; 27 7 409 418
19. Grazul-Bilska A. T., Johnson M. L., Bilski J. J., et al. Wound healing: the role of growth factors. Drugs Today (Barc): 2003; 39 10 787 800
20. Debus E. S., Schmidt K., Ziegler U. E., Thiede A. [The role of growth factors in wound healing]. Zentralbl Chir: 2000; 1 49 55
21. Steed D. L. The role of growth factors in wound healing. Surg Clin North Am: 1997; 77 3 575 586
22. Sobiczewska E., Szmigielski S. [The role of selected cell growth factors in the wound healing process]. Przegl Lek: 1997; 54 9 634 638
23. Greenhalgh D. G. The role of growth factors in wound healing. J Trauma: 1996; 41 1 159 167
24. Bennett N. T., Schultz G. S. Growth factors and wound healing: Part II. Role in normal and chronic wound healing. Am J Surg: 1993; 166 1 74 81
25. Kiritsy C. P., Lynch A. B., Lynch S. E. Role of growth factors in cutaneous wound healing: a review. Crit Rev Oral Biol Med: 1993; 4 5 729 760
26. Blitstein-Willinger E. The role of growth factors in wound healing. Skin Pharmacol: 1991; 4 3 175 182
27. Nemeth G. G., Bolander M. E., Martin G. R. Growth factors and their role in wound and fracture healing. Prog Clin Biol Res: 1988; 266 1 17
28. Robinson C. J. Growth factors: therapeutic advances in wound healing. Ann Med: 1993; 25 6 535 538
29. Zhang F., Waller W., Lineaweaver W. C. Growth factors and flap survival. Microsurgery: 2004; 24 3 162 167
30. Machens H. G., Niedworok C., Spanholtz T., Maichle A. PDGF gene therapy enhances expression of VEGF and bFGF genes. Plast Reconstr Surg: 2006; 118 3 820, author reply 820-821
31. Wang X. T., Liu P. Y., Tang J. B. PDGF gene therapy enhances expression of VEGF and bFGF genes and activates the NF-kappaB gene in signal pathways in ischemic flaps. Plast Reconstr Surg: 2006; 117 1 129 137, discussion 138-139
32. Folkman J., Shing Y. Angiogenesis. J Biol Chem: 1992; 267 16 10931 10934
33. Thurston G., Gale N. W. Vascular endothelial growth factor and other signaling pathways in developmental and pathologic angiogenesis. Int J Hematol: 2004; 80 1 7 20
34. Zhang F., Lineaweaver W. Acute and sustained effects of vascular endothelial growth factor on survival of flaps and skin grafts. Ann Plast Surg: 2011; 66 5 581 582
35. Padubidri A., Browne E. Jr. Effect of vascular endothelial growth factor (VEGF) on survival of random extension of axial pattern skin flaps in the rat. Ann Plast Surg: 1996; 37 6 604 611
36. Wei P., Li F. [The effect of vascular endothelial cell growth factor on survival of skin flap in rats]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi: 1997; 11 6 376 378
37. Zhang F., Oswald T., Lin S., et al. Vascular endothelial growth factor (VEGF) expression and the effect of exogenous VEGF on survival of a random flap in the rat. Br J Plast Surg: 2003; 56 7 653 659
38. Richter G. T., Fan C. Y., Ozgursoy O., McCoy J., Vural E. Effect of vascular endothelial growth factor on skin graft survival in Sprague-Dawley rats. Arch Otolaryngol Head Neck Surg: 2006; 132 6 637 641
39. Sun Q., Zheng Y., Ma T. [The effects of vascular endothelial growth factor on survival of reverse flow axial skin flaps]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi: 2007; 21 1 44 47
40. Kryger Z., Dogan T., Zhang F., et al. Effects of VEGF administration following ischemia on survival of the gracilis muscle flap in the rat. Ann Plast Surg: 1999; 43 2 172 178
41. Stebbins W. G., Fan C., Silver L., Chun J. K. Effect of VEGF on tail artery interpositional loop (TAIL) flap: a rodent model for flap prefabrication. J Reconstr Microsurg: 2005; 21 7 477 482
42. Zhang F., Fischer K., Komorowska-Timek E., et al. Improvement of skin paddle survival by application of vascular endothelial growth factor in a rat TRAM flap model. Ann Plast Surg: 2001; 46 3 314 319
43. Seify H., Bulky U., Jones G. Effect of vascular endothelial growth factor-induced angiogenesis on TRAM flap harvesting after abdominoplasty. Plast Reconstr Surg: 2003; 111 3 1212 1216
44. Zhang F., Brooks D., Chen W., Mustain W., Chen M. B., Lineaweaver W. C. Improvement of venous flap survival by application of vascular endothelial growth factor in a rat model. Ann Plast Surg: 2006; 56 6 670 673
45. Khan A., Ashrafpour H., Huang N., et al. Acute local subcutaneous VEGF165 injection for augmentation of skin flap viability: efficacy and mechanism. Am J Physiol Regul Integr Comp Physiol: 2004; 287 5 R1219 R1229
46. Miao W., Liang J., Luo S. [Comparison of effects of flap delay and vascular endothelial growth factor on the viability of the rat dorsal flap]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi: 2006; 20 5 530 533
47. Tetik Menevse G., Islamoglu K., Ege Ozgentas H. Expansion of surviving skin paddle of neurocutaneous island flaps in rats by VEGF. J Reconstr Microsurg: 2007; 23 2 99 105
48. Zhang Y., Mao J. S., Wang B. C., et al. [Effects on the survival of rat's abdominal axial skin flap after the combination of VEGF gene therapy and skin flap delay]. Zhonghua Zheng Xing Wai Ke Za Zhi: 2008; 24 1 39 41
49. Kryger Z., Zhang F., Dogan T., Cheng C., Lineaweaver W. C., Buncke H. J. The effects of VEGF on survival of a random flap in the rat: examination of various routes of administration. Br J Plast Surg: 2000; 53 3 234 239
50. Wang F., Zhao M., Huang B., et al. [Subcutaneous injection of plasmid VEGF gene: a method of gene therapy to enhance the viability of random skin flap]. Zhonghua Zheng Xing Wai Ke Za Zhi: 2002; 18 3 157 159
51. Yang L. W., Zhang J. X., Zeng L., et al. Vascular endothelial growth factor gene therapy with intramuscular injections of plasmid DNA enhances the survival of random pattern flaps in a rat model. Br J Plast Surg: 2005; 58 3 339 347
52. O'Toole G., MacKenzie D., Lindeman R., et al. Vascular endothelial growth factor gene therapy in ischaemic rat skin flaps. Br J Plast Surg: 2002; 55 1 55 58
53. Antonini A., Zacchigna S., Papa G., Novati F., Pascone M., Giacca M. Improved survival of rat ischemic cutaneous and musculocutaneous flaps after VEGF gene transfer. Microsurgery: 2007; 27 5 439 445
54. Wang L., Cen Y., Xiao H. [Studies on enhancement of transverse rectus abdominis musculocutaneous flap survival by recombinant adenovirus mediated vascular endothelial growth factor 165 gene]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi: 2005; 19 8 617 621
55. Giunta R. E., Holzbach T., Taskov C., et al. AdVEGF165 gene transfer increases survival in overdimensioned skin flaps. J Gene Med: 2005; 7 3 297 306
56. Michlits W., Mittermayr R., Schäfer R., Redl H., Aharinejad S. Fibrin-embedded administration of VEGF plasmid enhances skin flap survival. Wound Repair Regen: 2007; 15 3 360 367
57. Komorowska-Timek E., Timek T. A., Brevetti L. S., Zhang F., Lineaweaver W. C., Buncke H. J. The effect of single administration of vascular endothelial growth factor or L-arginine on necrosis and vasculature of the epigastric flap in the rat model. Br J Plast Surg: 2004; 57 4 317 325
58. Machens H. G., Salehi J., Weich H., et al. Angiogenic effects of injected VEGF165 and sVEGFR-1 (sFLT-1) in a rat flap model. J Surg Res: 2003; 111 1 136 142
59. Li Q. F., Reis E. D., Zhang W. X., Silver L., Fallon J. T., Weinberg H. Accelerated flap prefabrication with vascular endothelial growth factor. J Reconstr Microsurg: 2000; 16 1 45 49
60. Zhang F., Richards L., Angel M. F., et al. Accelerating flap maturation by vascular endothelium growth factorin a rat tube flap model. Br J Plast Surg: 2002; 55 1 59 63
61. Huang C. Y., Shen Z. Y. [Accelerated maturation of expanded prefabricated flaps by use of vascular endothelial growth factor and basic fibroblast growth factor in rabbits]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi: 2003; 17 4 293 297
62. Scalise A., Tucci M. G., Lucarini G., et al. Local rh-VEGF administration enhances skin flap survival more than other types of rh-VEGF administration: a clinical, morphological and immunohistochemical study. Exp Dermatol: 2004; 13 11 682 690
63. Zhang F., Yang F., Hu E. C., Sones W., Lei M., Lineaweaver W. C. Vascular endothelial growth factor gene therapy in improvement of skin paddle survival in a rat TRAM flap model. J Reconstr Microsurg: 2005; 21 6 391 396
64. Taub P. J., Marmur J. D., Zhang W. X., et al. Locally administered vascular endothelial growth factor cDNA increases survival of ischemic experimental skin flaps. Plast Reconstr Surg: 1998; 102 6 2033 2039
65. Taub P. J., Marmur J. D., Zhang W. X., et al. Effect of time on the viability of ischemic skin flaps treated with vascular endothelial growth factor (VEGF) cDNA. J Reconstr Microsurg: 1998; 14 6 387 390
66. Xiong B., Yi C. X., Guo J. L., Zhang Y. M., Feng X. L., Zhou W. D. [An experimental study on the survival of the anterior abdominal skin flap after VEGF cDNA administration]. Zhonghua Zheng Xing Wai Ke Za Zhi: 2003; 19 3 211 213
67. Xiong B., Yi C. X., Chen H. D., et al. [Vascular endothelial growth factor gene transfection and survival of the random skin flap in rats]. Di Yi Jun Yi Da Xue Xue Bao: 2004; 24 7 794 797
68. Liu P. Y., Tong W., Liu K., et al. Liposome-mediated transfer of vascular endothelial growth factor cDNA augments survival of random-pattern skin flaps in the rat. Wound Repair Regen: 2004; 12 1 80 85
69. Neumeister M. W., Song Y. H., Mowlavi A., Suchy H., Mathur A. Effects of liposome-mediated gene transfer of VEGF in ischemic rat gracilis muscle. Microsurgery: 2001; 21 2 58 62
70. Yu Y. S., Ye X. D., Shou L. [The therapy with rhVEGF gene for ischemic TRAM flap in rats]. Zhonghua Zheng Xing Wai Ke Za Zhi: 2003; 19 5 373 376
71. Gurunluoglu R., Ozer K., Skugor B., Lubiatowski P., Carnevale K., Siemionow M. Effect of transfection time on the survival of epigastric skin flaps pretreated with adenovirus encoding the VEGF gene. Ann Plast Surg: 2002; 49 2 161 169
72. Lubiatowski P., Goldman C. K., Gurunluoglu R., Carnevale K., Siemionow M. Enhancement of epigastric skin flap survival by adenovirus-mediated VEGF gene therapy. Plast Reconstr Surg: 2002; 109 6 1986 1993
73. Cui L., Li F. C., Zhang Q., Qian Y. L., Guan W. X. Effect of adenovirus-mediated gene transfection of vascular endothelial growth factor on survival of random flaps in rats. Chin J Traumatol: 2003; 6 4 199 204
74. Zacchigna S., Papa G., Antonini A., et al. Improved survival of ischemic cutaneous and musculocutaneous flaps after vascular endothelial growth factor gene transfer using adeno-associated virus vectors. Am J Pathol: 2005; 167 4 981 991
75. Li F. C., Cui L., Sun Y. X., Qian Y. L., Chen S. S., Guan W. X. [Effects of hVEGF cDNA on random skin flap via a replication-deficient adenovirus vector]. Zhonghua Zheng Xing Wai Ke Za Zhi: 2004; 20 6 434 438
76. Gurunluoglu R., Meirer R., Shafighi M., Huemer G. M., Yilmaz B., Piza-Katzer H. Gene therapy with adenovirus-mediated VEGF enhances skin flap prefabrication. Microsurgery: 2005; 25 5 433 441
77. Mittermayr R., Morton T., Hofmann M., Helgerson S., van Griensven M., Redl H. Sustained (rh)VEGF(165) release from a sprayed fibrin biomatrix induces angiogenesis, up-regulation of endogenous VEGF-R2, and reduces ischemic flap necrosis. Wound Repair Regen: 2008; 16 4 542 550
78. McKnight C. D., Winn S. R., Gong X., Hansen J. E., Wax M. K. Revascularization of rat fasciocutaneous flap using CROSSEAL with VEGF protein or plasmid DNA expressing VEGF. Otolaryngol Head Neck Surg: 2008; 139 2 245 249
79. Yi C. G., Guo S. Z., Zhang L. X., et al. [Promotion of the survival of ischemic skin flap by transplanted endothelial progenitor cells transfected with VEGF165 gene: an experimental study with mice]. Zhonghua Yi Xue Za Zhi: 2005; 85 7 473 478
80. Lasso J. M., Del Río M., García M., et al. Improving flap survival by transplantation of a VEGF-secreting endothelised scaffold during distal pedicle flap creation. J Plast Reconstr Aesthet Surg: 2007; 60 3 279 286
81. Zheng Y., Yi C., Xia W., et al. Mesenchymal stem cells transduced by vascular endothelial growth factor gene for ischemic random skin flaps. Plast Reconstr Surg: 2008; 121 1 59 69
82. Zheng Y., Yi C. G., He L. J., et al. [Effects of mouse NIH3T3 cells transfected with VEGF gene on neovascularization of ischemic flaps]. Zhonghua Wai Ke Za Zhi: 2007; 45 3 203 206
83. Liu P. Y., Liu K., Wang X. T., et al. Efficacy of combination gene therapy with multiple growth factor cDNAs to enhance skin flap survival in a rat model. DNA Cell Biol: 2005; 24 11 751 757
84. Ylä-Kotola T. M., Kauhanen S. C., Leivo I. V., Haglund C., Tukiainen E. Vascular endothelial growth factor and its receptors are expressed in human nerve grafts. J Reconstr Microsurg: 2011; 27 3 173 178
85. Lineaweaver W. C., Lei M. P., Mustain W., Oswald T. M., Cui D., Zhang F. Vascular endothelium growth factor, surgical delay, and skin flap survival. Ann Surg: 2004; 239 6 866 873, discussion 873-875
86. Lu X., Hao J., Wang Z. [Study on mechanism of the circulation reconstructing of skin flap after early-repeated short ischemia training]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi: 2006; 20 7 717 721
87. Brogi E., Wu T., Namiki A., Isner J. M. Indirect angiogenic cytokines upregulate VEGF and bFGF gene expression in vascular smooth muscle cells, whereas hypoxia upregulates VEGF expression only. Circulation: 1994; 90 2 649 652
88. Detmar M., Yeo K. T., Nagy J. A., et al. Keratinocyte-derived vascular permeability factor (vascular endothelial growth factor) is a potent mitogen for dermal microvascular endothelial cells. J Invest Dermatol: 1995; 105 1 44 50
89. Detmar M., Brown L. F., Berse B., et al. Hypoxia regulates the expression of vascular permeability factor/vascular endothelial growth factor (VPF/VEGF) and its receptors in human skin. J Invest Dermatol: 1997; 108 3 263 268
90. Shen H., Clauss M., Ryan J., et al. Characterization of vascular permeability factor/vascular endothelial growth factor receptors on mononuclear phagocytes. Blood: 1993; 81 10 2767 2773
91. Fong G. H., Rossant J., Gertsenstein M., Breitman M. L. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature: 1995; 376 6535 66 70
92. Gille H., Kowalski J., Li B., et al. Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J Biol Chem: 2001; 276 5 3222 3230
93. de Vries C., Escobedo J. A., Ueno H., Houck K., Ferrara N., Williams L. T. The fms-like tyrosine kinase, a receptor for vascular endothelial growth factor. Science: 1992; 255 5047 989 991
94. Gerber H. P., McMurtrey A., Kowalski J., et al. Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3′-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J Biol Chem: 1998; 273 46 30336 30343
95. Millauer B., Wizigmann-Voos S., Schnürch H., et al. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell: 1993; 72 6 835 846
96. Chen W., Zhang F., Chen M. B., Lineaweaver W. C. Expression of vascular endothelial growth factor receptor-2 in the muscle flap with ischemic injury in rats. J Surg Res: 2007; 140 1 45 49
97. Roberts D. M., Kearney J. B., Johnson J. H., Rosenberg M. P., Kumar R., Bautch V. L. The vascular endothelial growth factor (VEGF) receptor Flt-1 (VEGFR-1) modulates Flk-1 (VEGFR-2) signaling during blood vessel formation. Am J Pathol: 2004; 164 5 1531 1535
98. Dunk C., Ahmed A. Vascular endothelial growth factor receptor-2-mediated mitogenesis is negatively regulated by vascular endothelial growth factor receptor-1 in tumor epithelial cells. Am J Pathol: 2001; 158 1 265 273
99. Ahrendt G., Chickering D. E., Ranieri J. P. Angiogenic growth factors: A review for tissue engineering. Tissue Eng: 1998; 4 2 117 130
100. Boontheekul T., Mooney D. J. Protein-based signaling systems in tissue engineering. Curr Opin Biotechnol: 2003; 14 5 559 565
101. Yang R., Bunting S., Jin H. Effects of VEGF on hemodynamics and cardiac function: characterization and mechanisms. IDrugs: 2000; 3 11 1346 1352
102. Murohara T., Horowitz J. R., Silver M., et al. Vascular endothelial growth factor/vascular permeability factor enhances vascular permeability via nitric oxide and prostacyclin. Circulation: 1998; 97 1 99 107
103. Tucci M. G., Scalise A., Lucarini G., et al. rhVEGF and experimental rat skin flaps: systemic or local administration and morphological characteristics. Int J Artif Organs: 2001; 24 10 743 751
104. Vedder N. Flap physiology. In: Mathes S. J., Hentz V. R., eds. Plastic Surgery. Philadelphia Saunders-Elsevier: 2005; 486 490
105. Roberts W. G., Palade G. E. Increased microvascular permeability and endothelial fenestration induced by vascular endothelial growth factor. J Cell Sci: 1995; 108 Pt 6 2369 2379
106. Erdmann D., Sweis R., Wong M. S., et al. Vascular endothelial growth factor expression in pig latissimus dorsi myocutaneous flaps after ischemia reperfusion injury. Plast Reconstr Surg: 2003; 111 2 775 780
107. Erdmann D., Pippen A. M., Moquin K. J., et al. Immunohistochemical identification of vascular endothelial growth factor in pig latissimus dorsi musculocutaneous flaps following ischemia-reperfusion injury. Ann Plast Surg: 2004; 53 4 398 403
108. Roskoski R. Jr. VEGF receptor protein-tyrosine kinases: structure and regulation. Biochem Biophys Res Commun: 2008; 375 3 287 291
109. Pekala P., Marlow M., Heuvelman D., Connolly D. Regulation of hexose transport in aortic endothelial cells by vascular permeability factor and tumor necrosis factor-alpha, but not by insulin. J Biol Chem: 1990; 265 30 18051 18054
110. O'Connor D. S., Schechner J. S., Adida C., et al. Control of apoptosis during angiogenesis by survivin expression in endothelial cells. Am J Pathol: 2000; 156 2 393 398
111. Huang C. Y., Shen Z. Y. [Accelerated maturation of expanded prefabricated flaps by use of vascular endothelial growth factor and basic fibroblast growth factor in rabbits]. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi: 2003; 17 4 293 297
112. Pang Y., Lineaweaver W. C., Lei M. P., et al. Evaluation of the mechanism of vascular endothelial growth factor improvement of ischemic flap survival in rats. Plast Reconstr Surg: 2003; 112 2 556 564
113. Zhang F., Oswald T., Holt J., Gerzenshtein J., Lei M. P., Lineaweaver W. C. Regulation of inducible nitric oxide synthase in ischemic preconditioning of muscle flap in a rat model. Ann Plast Surg: 2004; 52 6 609 613
114. Topp S. G., Zhang F., Chatterjee T., Lineaweaver W. C. Role of nitric oxide in surgical flap survival. J Am Coll Surg: 2005; 201 4 628 639
115. Kane A. J., Barker J. E., Mitchell G. M., et al. Inducible nitric oxide synthase (iNOS) activity promotes ischaemic skin flap survival. Br J Pharmacol: 2001; 132 8 1631 1638
116. Furuta S., Vadiveloo P., Romeo-Meeuw R., Morrison W., Stewart A., Mitchell G. Early inducible nitric oxide synthase 2 (NOS 2) activity enhances ischaemic skin flap survival. Angiogenesis: 2004; 7 1 33 43
117. Ashrafpour H., Huang N., Neligan P. C., et al. Vasodilator effect and mechanism of action of vascular endothelial growth factor in skin vasculature. Am J Physiol Heart Circ Physiol: 2004; 286 3 H946 H954
118. Zhang F., Hu E. C., Gerzenshtein J., Lei M. P., Lineaweaver W. C. The expression of proinflammatory cytokines in the rat muscle flap with ischemia-reperfusion injury. Ann Plast Surg: 2005; 54 3 313 317
119. Zhang F., Hu E. C., Topp S., Lei M., Chen W., Lineaweaver W. C. Proinflammatory cytokines gene expression in skin flaps with arterial and venous ischemia in rats. J Reconstr Microsurg: 2006; 22 8 641 647
120. Lubiatowski P., Gurunluoglu R., Goldman C. K., Skugor B., Carnevale K., Siemionow M. Gene therapy by adenovirus-mediated vascular endothelial growth factor and angiopoietin-1 promotes perfusion of muscle flaps. Plast Reconstr Surg: 2002; 110 1 149 159
121. Segura M. M., Alba R., Bosch A., Chillón M. Advances in helper-dependent adenoviral vector research. Curr Gene Ther: 2008; 8 4 222 235
122. Yu Y. S., Ye X. D., Shou L. [The therapy with rhVEGF gene for ischemic TRAM flap in rats]. Zhonghua Zheng Xing Wai Ke Za Zhi: 2003; 19 5 373 376
123. McKnight C. D., Winn S. R., Gong X., Hansen J. E., Wax M. K. Revascularization of rat fasciocutaneous flap using CROSSEAL with VEGF protein or plasmid DNA expressing VEGF. Otolaryngol Head Neck Surg: 2008; 139 2 245 249
124. Kubota Y., Kishi K., Satoh H., Tanaka T., Nakajima H., Nakajima T. Transplanted endothelial progenitor cells augment the survival areas of rat dorsal flaps. Cell Transplant: 2003; 12 6 647 657
125. Xie S. T., Chen B., Tao K., Han J. T., Wang H. T. [The study on EPC originated from human umbilical cord blood promoting neovascularization in ischemic skin flap]. Zhonghua Zheng Xing Wai Ke Za Zhi: 2007; 23 3 206 208
126. Paletta C., Pokorny J., Rumbolo P. Skin Grafts. In: Mathes S., Hentz V., eds. Mathes Plastic Surgery. Philadelphia WB Saunders: 2006; 263 316