Microvascular morphometrics of the hypophysis and pituitary tumors: From bench to operating theatre

Microvascular Research

Volumn 89, Issue , 2013, Pages 7-14

  Di Ieva, Antonio ^a   Weckman, Andrea ^a   Di Michele, Joseph ^a   Rotondo, Fabio ^a   Grizzi, Fabio ^b   Kovacs, Kalman ^a   Cusimano, Michael D ^a  

^a ST MICHAEL'S HOSPITAL   (Canada)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; BLOOD CLOTTING FACTOR 8; CD31 ANTIGEN; CD34 ANTIGEN; DOPAMINE RECEPTOR STIMULATING AGENT; ENDOGLIN; INDOCYANINE GREEN; PEGVISOMANT; SOMATOSTATIN DERIVATIVE; TEMOZOLOMIDE; ULEX EUROPAEUS AGGLUTININ; VASCULOTROPIN; VON WILLEBRAND FACTOR;

ACROMEGALY; ANGIOGENESIS; ANTIANGIOGENIC THERAPY; CANCER PROGNOSIS; CAPILLARY DENSITY; HUMAN; HYPOPHYSIS; HYPOPHYSIS ADENOMA; HYPOPHYSIS TUMOR; IMMUNOHISTOCHEMISTRY; LASER DOPPLER FLOWMETRY; MICROVASCULATURE; MORPHOMETRICS; NEUROSURGERY; NONHUMAN; PATHOPHYSIOLOGY; PITUITARY CARCINOMA; PRIORITY JOURNAL; PROLACTINOMA; QUANTITATIVE ANALYSIS; REVIEW; TUMOR VASCULARIZATION;

ADENOMA; ANGIOGENESIS INHIBITORS; ANTIGENS, CD; ANTIGENS, CD34; BIOLOGICAL MARKERS; COMPUTER SIMULATION; DISEASE PROGRESSION; FRACTALS; HUMANS; IMMUNOHISTOCHEMISTRY; MICROCIRCULATION; MICROVESSELS; NEOPLASM METASTASIS; NEOVASCULARIZATION, PATHOLOGIC; PITUITARY GLAND; PITUITARY NEOPLASMS; RECEPTORS, CELL SURFACE;

EID: 84883159611     PISSN: 00262862     EISSN: 10959319     Source Type: Journal    
DOI: 10.1016/j.mvr.2013.04.009     Document Type: Review

References (104)

1. Baish J.W., Jain R.K. Cancer, angiogenesis and fractals. Nat. Med. 1998, 4:984.
2. Baish J.W., Jain R.K. Fractals and cancer. Cancer Res. 2000, 60:3683-3688.
3. Baish J.W., Gazit Y., Berk D.A., Nozue M., Baxter L.T., Jain R.K. Role of tumor vascular architecture in nutrient and drug delivery: an invasion percolation-based network model. Microvasc. Res. 1996, 51:327-346.
4. Balamurugan S., Agrawal A., Kato Y., Sano H., et al. Intra operative indocyanine green video-angiography in cerebrovascular surgery: an overview with review of literature. Asian J. Neurosurg. 2011, 6:88-93.
5. Batchelor T.T., Sorensen A.G., di Tomaso E., Zhang W.T., Duda D.G., Cohen K.S., Kozak K.R., Cahill D.P., Chen P.J., Zhu M., Ancukiewicz M., Mrugala M.M., Plotkin S., Drappatz J., Louis D.N., Ivy P., Scadden D.T., Benner T., Loeffler J.S., Wen P.Y., Jain R.K. AZD2171, a pan-VEGF receptor tyrosine kinase inhibitor, normalizes tumor vasculature and alleviates edema in glioblastoma patients. Cancer Cell 2007, 11:83-95.
6. Bochner B.H., Cote R.J., Weidner N., Groshen S., Chen S.C., Skinner D.G., Nichols P.W. Angiogenesis in bladder cancer: relationship between microvessel density and tumor prognosis. J. Natl. Cancer Inst. 1995, 87:1603-1612.
7. Borit A., Brooks T.E., Ordóñez N.G., Kakulas B.A. Central neural antigens: detection and diagnostic application. Crit. Rev. Clin. Lab. Sci. 1986, 23:219-243.
8. Buchfelder M. Management of aggressive pituitary adenomas: current treatment strategies. Pituitary 2009, 12:256-260.
9. Cheifetz S., Bellón T., Calés C., Vera S., Bernabeu C., Massagué J., Letarte M. Endoglin is a component of the transforming growth factor-beta receptor system in human endothelial cells. J. Biol. Chem. 1992, 267:19027-19030.
10. Cross S.S. The application of fractal geometric analysis to microscopic images. Micron 1994, 25:101-113.
11. Cross S.S. Fractals in pathology. J. Pathol. 1997, 182:1-8.
12. Dallas N.A., Samuel S., Xia L., Fan F., Gray M.J., Lim S.J., Ellis L.M. Endoglin (CD105): a marker of tumor vasculature and potential target for therapy. Clin. Cancer Res. 2008, 14:1931-1937.
13. DeLisser H.M., Newman P.J., Albeida S.M. Molecular and functional aspects of PECAM-1/CD31. Immunol. Today 1994, 15:490-495.
14. Di Ieva A. Angioarchitectural morphometrics of brain tumors: are there any potential histopathological biomarkers?. Microvasc. Res. 2010, 80:522-533.
15. Di Ieva A. Fractal analysis of microvascular networks in malignant brain tumors. Clin. Neuropathol. 2012, 31:342-351.
16. Di Ieva A., Bruner E., Widhalm G., Minchev G., Tschabitscher M., Grizzi F. Computer-assisted and fractal-based morphometric assessment of microvascularity in histological specimens of gliomas. Sci. Rep. 2012, 2:429. 10.1038/srep00429.
17. Di Ieva A., Matula C., Grizzi F., Grabner G., Trattnig S., Tschabitsher M. Fractal analysis of the susceptibility weighted imaging patterns in malignant brain tumors during antiangiogenic treatment: technical report on four cases serially imaged by 7T magnetic resonance during a period of four weeks. World Neurosurg. 2012, 77:711-721. 785.e.
18. Di Ieva A., Grizzi F., Ceva-Grimaldi G., Russo C., Gaetani P., Aimar E., Levi D., Pisano P., Tancioni F., Nicola G., Tschabitscher M., Dioguardi N., Baena R.R. Fractal dimension as a quantitator of the microvasculature of normal and adenomatous pituitary tissue. J. Anat. 2007, 211:673-680.
19. Di Ieva A., Grizzi F., Gaetani P., Goglia U., Tschabitscher M., Mortini P., Rodriguez y Baena R. Euclidean and fractal geometry of microvascular networks in normal and neoplastic pituitary tissue. Neurosurg. Rev. 2008, 31:271-281.
20. Di Ieva A., Grizzi F., Ceva-Grimaldi G., Aimar E., Serra S., Pisano P., Lorenzetti M., Tancioni F., Gaetani P., Crotti F., Tschabitsher M., Matula C., Rodriguez y Baena R. The microvascular network of the pituitary gland: a model for the application of fractal geometry to the analysis of angioarchitecture and angiogenesis of brain tumors. J. Neurosurg. Sci. 2010, 54:49-54.
21. Di Ieva A., Grizzi F., Sherif C., Matula C., Tschabitscher M. Angioarchitectural heterogeneity in human glioblastoma multiforme: a fractal-based histopathological assessment. Microvasc. Res. 2011, 81:222-230.
22. Di Ieva A., Göd S., Grabner G., Grizzi F., Sherif C., Matula C., Tschabitscher M., Trattnig S. Three-dimensional susceptibility-weighted imaging at 7T using fractal-based quantitative analysis to grade gliomas. Neuroradiology 2013, 55:35-40.
23. Ding S., Li C., Lin S., Yang Y., Liu D., Han Y., Zhang Y., Li L., Zhou L., Kumar S. Comparative evaluation of microvessel density determined by CD34 or CD105 in benign and malignant gastric lesions. Hum. Pathol. 2006, 37:861-866.
24. Döllinger J.W., Metzler R., Nonnenmacher T.F. Bi-asymptotic fractals: fractals between lower and upper bounds. J. Phys. A Math. Gen. 1998, 31:3839-3847.
25. Duff S.E., Li C., Garland J.M., Kumar S. CD105 is important for angiogenesis: evidence and potential applications. FASEB 2003, 17:984-992.
26. Feder J. Fractals (Physics of Solids and Liquids) 1988, Plenum Press, New York.
27. Folkman J. Anti-angiogenesis: new concept for therapy of solid tumors. Ann. Surg. 1972, 175:409-416.
28. Folkman J. What is the evidence that tumors are angiogenesis dependent?. J. Natl. Cancer Inst. 1990, 82:4-6.
29. Gasparini G., Bevilacqua P., Bonoldi E., Testolin A., Galassi A., Verderio P., Boracchi P., Guglielmi R.B., Pezzella F. Predictive and prognostic markers in a series of patients with head and neck squamous cell invasive carcinoma treated with concurrent chemoradiation therapy. Clin. Cancer Res. 1995, 1:1375-1383.
30. Gazit Y., Baish J.W., Safabakhsh N., Leunig M., Baxter L.T., Jain R.K. Fractal characteristics of tumor vascular architecture during tumor growth and regression. Microcirculation 1997, 4:395-402.
31. Gillam M.P., Molitch M.E., Lombardi G., Colao A. Advances in the treatment of prolactinomas. Endocr. Rev. 2006, 27:485-534.
32. Goel S., Duda D.G., Xu L., Munn L.L., Boucher Y., Fukumura D., Jain R.K. Normalization of the vasculature for treatment of cancer and other diseases. Physiol. Rev. 2011, 91:1071-1121.
33. Goel S., Fukumura D., Jain R.K. Normalization of the tumor vasculature through oncogenic inhibition: an emerging paradigm in tumor biology. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E1214.
34. Goel S., Wong A.H., Jain R.K. Vascular normalization as a therapeutic strategy for malignant and nonmalignant disease. Cold Spring Harb.Perspect. Med. 2012, 10.1101/cshperspect.a006486.
35. Gorczyca W., Hardy J. Arterial supply of the human anterior pituitary gland. Neurosurgery 1987, 20:369-378.
36. Gorczyca W., Hardy J. Microadenomas of the human pituitary and their vascularization. Neurosurgery 1988, 22:1-6.
37. Grizzi F., Russo C., Colombo P., Franceschini B., Frezza E.E., Cobos E., Chiriva-Internati M. Quantitative evaluation and modeling of two-dimensional neovascular network complexity: the surface fractal dimension. BMC Cancer 2005, 5:14-22.
38. Grizzi F., Colombo P., Taverna G., Chiriva-Internati M., Cobos E., Graziotti P., Muzzio P.C., Dioguardi N. Geometry of human vascular system: is it an obstacle for quantifying antiangiogenic therapies?. Appl. Immunohistochem. Mol. Morphol. 2007, 15:134-139.
39. Grizzi F., Weber C., Di Ieva A. Antiangiogenic strategies in medulloblastoma: reality or mystery. Pediatr. Res. 2008, 63:584-590.
40. Gueorguiev M., Grossman A.B. Pituitary tumors in 2010: a new therapeutic era for pituitary tumors. Nat. Rev. Endocrinol. 2011, 7:71-73.
41. Hicklin D.J., Ellis L.M. Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis. J. Clin. Oncol. 2005, 23:1011-1027.
42. Hlatky L., Hahnfeldt P., Folkman J. Clinical application of antiangiogenic therapy: microvessel density, what it does and doesn't tell us. J. Natl. Cancer Inst. 2002, 94:883-893.
43. Holthöfer H., Virtanen I., Kariniemi A.L., Hormia M., Linder E., Miettinen A. Ulex europaeus I lectin as a marker for vascular endothelium in human tissues. Lab. Invest. 1982, 47:60-66.
44. Hong H., Yang Y., Zhang Y., Engle J.W., Barnhart T.E., Nickles R.J., Leigh B.R., Cai W. Positron emission tomography imaging of CD105 expression during tumor angiogenesis. Eur. J. Nucl. Med. Mol. Imaging 2011, 38:1335-1343.
45. Izumi Y., Xu L., di Tomaso E., Fukumura D., Jain R.K. Tumour biology: herceptin acts as an anti-angiogenic cocktail. Nature 2002, 416:279-280.
46. Jaffe E.A. Synthesis of factor VIII by endothelial cells. Ann. N. Y. Acad. Sci. 1982, 401:163-170.
47. Jain R.K. Normalizing tumor vasculature with anti-angiogenic therapy: a new paradigm for combination therapy. Nat. Med. 2001, 7:987-989.
48. Jain R.K. Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science 2005, 307:58-62.
49. Jain R.K., Batchelor T.T., Duda D.G., Willet G.C. Normalization of Tumor Vasculature and Microenvironment. Antiangiogenic Agents in Cancer Therapy 2008, 261-276. Humana Press, New Jersey. 2nd edn. B.A. Teicher, L.M. Ellis (Eds.).
50. Jain R.K., Duda D.G., Willett C.G., Sahani D.V., Zhu A.X., Loeffler J.S., Batchelor T.T., Sorensen A.G. Biomarkers of response and resistance to antiangiogenic therapy. Nat. Rev.Clin. Oncol. 2009, 6:327-338.
51. Jasek E., Furgal-Borzych A., Lis G.J., Litwin J.A., Rzepecka-Wozniak E., Trela F. Microvessel density and area in pituitary microadenomas. Endocr. Pathol. 2009, 20:221-226.
52. Jugenburg M., Kovacs K., Stefaneanu L., Scheithauer B.W. Vasculature in nontumorous hypophyses, pituitary adenomas, and carcinomas: a quantitative morphologic study. Endocr. Pathol. 1995, 6:115-124.
53. Kamoun W.S., LeY C.D., Farrar C.T., Duyverman A.M., Lahdenranta J., Lacorre D.A., Batchelor T.T., Di Tomaso E., Duda D.G., Munn L.L., Fukumura D., Sorensen A.G., Jain R.K. Edema control by cediranib, a vascular endothelial growth factor receptor-targeted kinase inhibitor, prolongs survival despite persistent brain tumor growth in mice. J. Clin. Oncol. 2009, 27:2542-2552.
54. Kim E.H., Cho J.M., Chang J.H., Kim S.H., Lee K.S. Application of intraoperative indocyanine green videoangiography to brain tumor surgery. Acta Neurochir. 2011, 153:1487-1495.
55. Kirchner L.M., Schimdt S.P., Gruber B.S. Quantitation of angiogenesis in the chick chorioallantoic membrane model using fractal analysis. Microvasc. Res. 1996, 51:2-14.
56. Kovacs K., Horvath E. Tumors of the pituitary gland. Atlas of Tumor Pathology (second series) 1986, 1-264. Armed Forces Institute of Pathology, Washington.
57. Krause D., Fackler M., Civin C., May W.S. CD34: structure, biology, and clinical utility. Blood 1996, 87:1-13.
58. Panvascular Medicine: Integrated Clinical Management 2002, Springer-Verlag, Berlin. P. Lanzer, E.J. Topol (Eds.).
59. Litvack Z.N., Zada G., Laws E.R. Indocyanine green fluorescence endoscopy for visual differentiation of pituitary tumor from surrounding structures. J. Neurosurg. 2012, 116:935-941.
60. Losa G.A. The fractal geometry of life. Riv. Biol. 2009, 102:29-59.
61. Losa G.A., Nonnenmacher T.F. Self-similarity and fractal irregularity in pathologic tissues. Mod. Pathol. 1996, 9:174-182.
62. Mancardi D., Varetto G., Bucci E., Maniero F., Guiot C. Fractal parameters and vascular networks: facts & artifacts. Theor. Biol. Med. Model. 2008, 10.1186/1742-4682-5-12.
63. Mandelbrot B.B. The Fractal Geometry of Nature 1983, WH Freeman, New York.
64. Marioni G., D'Alessandro E., Giacomelli L., Staffieri A. CD105 is a marker of tumour vasculature and a potential target for the treatment of head and neck squamous cell carcinoma. J. Oral Pathol. Med. 2010, 39:361-367.
65. McKay T.L., Gedeon D.J., Vickerman M.B., Hylton A.G., Ribita D., Olar H.H., Kaiser P.K., Parsons-Wingerter P. Selective inhibition of angiogenesis in small blood vessels and decrease in vessel diameter throughout the vascular tree by triamcinolone acetonide. Invest. Ophthalmol. Vis. Sci. 2008, 49:1184-1190.
66. Miettinen M. Immunohistochemistry in tumour diagnosis. Ann. Med. 1993, 25:221-233.
67. Mukai K., Rosai J., Burgdorf W. Localization of factor VIII-related antigen in vascular endothelial cells using an immunoperoxidase method. Am. J. Surg. Pathol. 1980, 4:273-276.
68. Nadali G., De Wynter E.A., Testa N.G. CD34 cell separation: from basic research to clinical applications. Int. J. Clin. Lab. Res. 1995, 25:121-127.
69. Nassiri F., Cusimano M.D., Scheithauer B.W., Rotondo F., Fazio A., Yousef G.M., Syro L.V., Kovacs K., Lloyd R.V. Endoglin (CD105): a review of its role in angiogenesis and tumor diagnosis, progression and therapy. Anticancer. Res. 2011, 31:2283-2290.
70. Nassiri F., Cusimano M.D., Scheithauer B.W., Rotondo F., Fazio A., Syro L.V., Kovacs K., Lloyd R.V. Prolactinomas: diagnosis and treatment. Expert. Rev. Endocrinol. Metab. 2012, 7:233-241.
71. Netto G.C., Bleil C.B., Hilbig A., Coutinho L.M. Immunohistochemical evaluation of the microvascular density through the expression of TGF-β (CD 105/endoglin) and CD 34 receptors and expression of the vascular endothelial growth factor (VEGF) in oligodendrogliomas. Neuropathology 2008, 28:17-23.
72. Niveiro M., Aranda F.I., Peiró G., Alenda C., Picó A. Immunohistochemical analysis of tumor angiogenic factors in human pituitary adenomas. Hum. Pathol. 2005, 36:1090-1095.
73. Pichard C., Gerber S., Laloi M., Kujas M., Clemenceau S., Ponvert D., Bruckert E., Turpin G. Pituitary carcinoma: report of an exceptional case and review of the literature. J. Endocrinol. Invest. 2002, 25:65-72.
74. Pizarro C.B., Oliveira M.C., Pereira-Lima J.F., Leaes C.G., Kramer C.K., Schuch T., Barbosa-Coutinho L.M., Ferreira N.P. Evaluation of angiogenesis in 77 pituitary adenomas using endoglin as a marker. Neuropathology 2009, 29:40-44.
75. Preusser M., Heinzl H., Gelpi E., Schonegger K., Haberler C., Birner P., Marosi C., Hegi M., Gorlia T., Hainfellner J.A. Histopathologic assessment of hot-spot microvessel density and vascular patterns in glioblastoma: poor observer agreement limits clinical utility as prognostic factors. Cancer 2006, 107:162-170.
76. Ragel B.T., Couldwell W.T. Pituitary carcinoma: a review of the literature. Neurosurg. Focus. 2004, 16:E7.
77. Righi M., Giacomini A., Lavazza C., Sia D., Carlo-Stella C., Gianni A.M. A computational approach to compare microvessel distributions in tumors following antiangiogenic treatments. Lab. Invest. 2009, 89:1063-1070.
78. Ríus C., Smith J.D., Almendro N., Langa C., Botella L.M., Marchuck D.A., Vary C.P., Bernabeu C. Cloning of the promoter region of human endoglin, the target gene for hereditary hemorrhagic telangiectasia type 1. Blood 1998, 92:4677-4690.
79. Rotondo F., Sharma S., Scheithauer B.W., Horvath E., Syro L.V., Cusimano M.D., Nassiri F., Yousef G.M., Kovacs K. Endoglin and CD-34 immunoreactivity in the assessment of microvessel density in normal pituitary and adenoma subtypes. Neoplasma 2010, 57:590-593.
80. Sánchez-Elsner T., Botella L.M., Velasco B., Langa C., Bernabéu C. Endoglin expression is regulated by transcriptional cooperation between the hypoxia and transforming growth factor-beta pathways. J. Biol. Chem. 2002, 277:43799-43808.
81. Schechter J. Ultrastructural changes in the capillary bed of human pituitary tumors. Am. J. Pathol. 1972, 67:109-126.
82. Schreiber I., Buchfelder M., Droste M., Forssmann K., Mann K., Saller B., Strasburger C.J. Treatment of acromegaly with the GH receptor antagonist pegvisomant in clinical practice: safety and efficacy evaluation from the German Pegvisomant Observational Study. Eur. J. Endocrinol. 2007, 156:75-82.
83. Seaman M.E., Peirce S.M., Kelly K. Rapid analysis of vessel elements (RAVE): a tool for studying physiologic, pathologic and tumor angiogenesis. PLoS One 2011, 10.1371/journal.pone.0020807.
84. Steinmeier R., Fahlbusch R., Powers A.D., Dötterl A., Buchfelder M. Pituitary microcirculation: physiological aspects and clinical implications. A laser-Doppler flow study during transsphenoidal adenomectomy. Neurosurgery 1991, 29:47-54.
85. Syro L.V., Ortiz L.D., Scheithauer B.W., Lloyd R.V., Lau Q., Gonzalez R., Uribe H., Cusimano M.D., Kovacs K., Horvath E. Treatment of pituitary neoplasms with temozolomide. Cancer 2011, 117:454-462.
86. Tong R.T., Boucher Y., Kozin S.V., Winkler F., Hicklin D.J., Jain R.K. Vascular normalization by vascular endothelial growth factor receptor 2 blockade induces a pressure gradient across the vasculature and improves drug penetration in tumors. Cancer Res. 2004, 64:3731-3736.
87. Turner H., Nagy Z., Gatter K., Esiri M., Harris A., Wass J. Angiogenesis in pituitary adenomas-relationship to endocrine function, treatment and outcome. J. Endocrinol. 2000, 165:475-481.
88. Turner H., Nagy Z., Gatter K., Esiri M., Harris A., Wass J. Angiogenesis in pituitary adenomas and the normal pituitary gland. J. Clin. Endocrinol. Metab. 2000, 85:1159-1162.
89. Turner H., Nagy Z., Gatter K., Esiri M., Wass J., Harris A. Proliferation, bcl-2 expression and angiogenesis in pituitary adenomas: relationship to tumour behaviour. Br. J. Cancer 2000, 82:1441-1445.
90. Vakoc B.J., Lanning R.M., Tyrrell J.A., Padera T.P., Bartlett L.A., Stylianopoulos T., Munn L.L., Tearney G.J., Fukumura D., Jain R.K., Bouma B.E. Three-dimensional microscopy of the tumor microenvironment in vivo using optical frequency domain imaging. Nat. Med. 2009, 15:1219-1223.
91. van der Loos C.M., Meijer-Jorna L.B., Broekmans M.E., Ploegmakers H.P., Teeling P., de Boer O.J., van der Wal A.C. Anti-human vascular endothelial growth factor (VEGF) antibody selection for immunohistochemical staining of proliferating blood vessels. J. Histochem. Cytochem. 2010, 58:109-118.
92. Verhoelst E., De Ketelaere B., Bruggeman V., Villamor E., Decuypere E., De Baerdemaeker J. Development of a fast, objective, quantitative methodology to monitor angiogenesis in the chicken chorioallantoic membrane during development. Int. J. Dev. Biol. 2011, 55:85-92.
93. Vermeulen P., Verhoeven D., Fierens H., Hubens G., Goovaerts G., Van Marck E., De Bruijn E.A., Van Oosterom A.T., Dirix L.Y. Microvessel quantification in primary colorectal carcinoma: an immunohistochemical study. Br. J. Cancer 1995, 71:340-343.
94. Vermeulen P., Gasparini G., Fox S., Toi M., Martin L., McCulloch P., Pezzella F., Viale G., Weidner N., Harris A.L., Dirix L.Y. Quantification of angiogenesis in solid human tumours: an international consensus on the methodology and criteria of evaluation. Eur. J. Cancer 1996, 32:2474-2484.
95. Viacava P., Gasperi M., Acerbi G., Manetti L., Cecconi E., Bonadio A.G., Naccarato A.G., Acerbi F., Parenti G., Lupi I., Genovesi M., Martino E. Microvascular density and vascular endothelial growth factor expression in normal pituitary tissue and pituitary adenomas. J. Endocrinol. Invest. 2003, 26:23-28.
96. Vickerman M.B., Keith P.A., McKay T.L., Gedeon D.J., Watanabe M., Montano M., Karunamuni G., Kaiser P.K., Sears J.E., Ebrahem Q., Ribita D., Hylton A.G., Parsons-Wingerter P. VESGEN 2D: automated, user-interactive software for quantification and mapping of angiogenic and lymphangiogenic trees and networks. Anat. Rec. 2009, 292:320-332.
97. Vidal S., Scheithauer B.W., Kovacs K. Vascularity in nontumorous human pituitaries and incidental microadenomas: a morphometric study. Endocr. Pathol. 2000, 11:215-227.
98. Vidal S., Kovacs K., Horvath E., Scheithauer B., Kuroki T., Lloyd R. Microvessel density in pituitary adenomas and carcinomas. Virchows Arch. 2001, 438:595-602.
99. Vidal S., Horvath E., Kovacs K., Lloyd R.V., Scheithauer B.W. Microvascular structural entropy: a novel approach to assess angiogenesis in pituitary tumors. Endocr. Pathol. 2003, 14:239-247.
100. Weidner N., Semple J.P., Welch W.R., Folkman J. Tumor angiogenesis and metastasis - correlation in invasive breast carcinoma. N. Engl. J. Med. 1991, 324:1-8.
101. Winkler F., Kozin S.V., Tong R.T., Chae S.S., Booth M.F., Garkavtsev I., Xu L., Hicklin D.J., Fukumura D., di Tomaso E., Munn L.L., Jain R.K. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 2004, 6:553-563.
102. Yamada S., Takada K. Angiogenesis in pituitary adenomas. Microsc. Res. Tech. 2003, 60:236-243.
103. Yilmazer D., Han Ü., Önal B. A comparison of the vascular density of VEGF expression with microvascular density determined with CD34 and CD31 staining and conventional prognostic markers in renal cell carcinoma. Int. Urol. Nephrol. 2007, 39:691-698.
104. Zhang Y., He N., Zhou J., Chen Y. The relationship between MRI invasive features and expression of EMMPRIN, galectin-3, and microvessel density in pituitary adenoma. Clin. Imaging 2011, 35:165-173.