Spectral imaging reveals microvessel physiology and function from anastomoses to thromboses

Journal of Biomedical Optics

Volumn 15, Issue 1, 2010, Pages

  Wankhede, Mamta ^a   Agarwal, Nikita ^a   Fraga Silva, Rodrigo A ^b   Dedeugd, Casey ^a   Raizada, Mohan K ^b   Paul Oh, S ^b,c,d   Sorg, Brian S ^a  

^a University of Florida   (United States)

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

^d University of Medicine   (South Korea)

Author keywords

Arteriovenous; Hemoglobin; In vivo; Microscopy; Oxygen; Tumor

Indexed keywords

ABNORMAL VASCULAR REMODELING; ANGIOGENESIS; ARTERIOVENOUS; ARTERIOVENOUS MALFORMATION; DIRECT IMAGING; HEMOGLOBIN SATURATION; IN VIVO; INTRAVITAL MICROSCOPY; MICROVASCULAR; MICROVASCULAR THROMBOSIS; MOUSE MODELS; OPTICAL TECHNIQUE; OXYGEN TRANSPORT; QUANTITATIVE IMAGING; SPECTRAL IMAGING; SPECTRAL IMAGING SYSTEM; TEMPORAL RESOLUTION; WINDOW CHAMBERS;

HEMOGLOBIN; HEMOGLOBIN OXYGEN SATURATION; MAMMALS; OXYGEN; OXYGENATION; PHYSIOLOGY; TUMORS;

BLOOD VESSELS;

HEMOGLOBIN; OXYGEN;

ANIMAL; ARTERIOVENOUS FISTULA; ARTICLE; BREAST TUMOR; CANCER TRANSPLANTATION; DISEASE MODEL; FEMALE; IMAGE PROCESSING; IMMUNOLOGICAL PROCEDURES; METABOLISM; METHODOLOGY; MICROVASCULATURE; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NUDE MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; RENDU OSLER WEBER DISEASE; SPECTROSCOPY; THROMBOSIS; TUMOR CELL LINE;

ANIMALS; ARTERIOVENOUS ANASTOMOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; FEMALE; HEMOGLOBINS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICE; MICE, NUDE; MICROVESSELS; NEOPLASM TRANSPLANTATION; NEOVASCULARIZATION, PATHOLOGIC; OXYGEN; SKIN WINDOW TECHNIQUE; SPECTRUM ANALYSIS; TELANGIECTASIA, HEREDITARY HEMORRHAGIC; THROMBOSIS;

EID: 77953159801     PISSN: 10833668     EISSN: 15602281     Source Type: Journal    
DOI: 10.1117/1.3316299     Document Type: Article

References (90)

1. B. N. Perry and J. L. Arbiser, "The duality of angiogenesis: implications for therapy of human disease", J. Invest. Dermatol. 126, 2160-2166 (2006). (Pubitemid 44413161)
2. Z. K. Otrock, R. A. R. Mahfouz, J. A. Makarem, and A. I. Shamseddine, "Understanding the biology of angiogenesis: review of the most important molecular mechanisms", Blood Cells Mol. Dis. 39, 212-220 (2007). (Pubitemid 47126926)
3. P. Carmeliet and R. K. Jain, "Angiogenesis in cancer and other diseases", Nature 407, 249-257 (2000).
4. M. W. Dewhirst, "Angiogenesis and blood flow in solid tumors", in Drug Resistance in Oncology, B. A. Teicher, Ed., pp. 3-23, Marcel Dekker, New York (1993).
5. B. A. Warren, "The vascular morphology of tumors", in Tumor Blood Circulation: Angiogenesis, Vascular Morphology and Blood Flow of Experimental and Human Tumors, H.-I. Peterson, Ed., pp. 1-47, CRC Press, Inc., Boca Raton, FL (1979).
6. M. Simons, "Angiogenesis, arteriogenesis, and diabetes-paradigm reassessed?" J. Am. Coll. Cardiol. 46, 835-837 (2005).
7. A. Martin, M. R. Komada, and D. C. Sane, "Abnormal angiogenesis in diabetes mellitus", Med. Res. Rev. 23, 117-145 (2003). (Pubitemid 36241095)
8. J. F. Carvalho, M. Blank, and Y. Shoenfeld, "Vascular endothelial growth factor (VEGF) in autoimmune diseases", J. Clin. Immunol. 27, 246-256 (2007). (Pubitemid 46790822)
9. J. Bainbridge, B. Sivakumar, and E. Paleolog, "Angiogenesis as a therapeutic target in arthritis: lessons from oncology", Curr. Pharm. Des. 12, 2631-2644 (2006).
10. R. S. Azfar and J. M. Gelfand, "Psoriasis and metabolic disease: epidemiology and pathophysiology", Curr. Opin. Rheumatol. 20, 416-422 (2008).
11. P. Gargiulo, C. Giusti, D. Pietrobono, D. La Torre, D. Diacono, and G. Tamburrano, "Diabetes mellitus and retinopathy", Dig. Liver Dis. 36(Suppl. 1), S101-S105 (2004). (Pubitemid 41115497)
12. U. Wegewitz, I. Göhring, and J. Spranger, "Novel approaches in the treatment of angiogenic eye disease", Curr. Pharm. Des. 11, 2311-2330 (2005). (Pubitemid 40872700)
13. K.-I. O'goshi and J. Serup, "Safety of sodium fluorescein for in vivo study of skin", Skin Res. Technol. 12, 155-161 (2006). (Pubitemid 43985008)
14. E. Werkmeister, H. Kerdjoudj, L. Marchal, J. F. Stoltz, and D. Dumas, "Multiphoton microscopy for blood vessel imaging: new noninvasive tools (Spectral, SHG, FLIM)", Clin. Hemorheol Microcirc 37, 77-88 (2007). (Pubitemid 47015814)
15. C. B. Schaffer, B. Friedman, N. Nishimura, L. F. Schroeder, P. S. Tsai, F. F. Ebner, P. D. Lyden, and D. Kleinfeld, "Two-photon imaging of cortical surface microvessels reveals a robust redistribution in blood flow after vascular occlusion", PLoS Biol. 4, e22 (2006).
16. C. C. Reyes-Aldasoro, I. Wilson, V. E. Prise, P. R. Barber, M. Ameer-Beg, B. Vojnovic, V. J. Cunningham, and G. M. Tozer, "Estimation of apparent tumor vascular permeability from multiphoton fluorescence microscopic images of P22 rat sarcomas in vivo", Microcirculation (N. Y.) 15, 65-79 (2008).
17. D. Fu, T. E. Matthews, T. Ye, I. R. Piletic, and W. S. Warren, "Labelfree in vivo optical imaging of microvasculature and oxygenation level", J. Biomed. Opt. 13, 040503 (2008).
18. B. Choi, N. M. Kang, and J. S. Nelson, "Laser speckle imaging for monitoring blood flow dynamics in the in vivo rodent dorsal skin fold model", Microvasc. Res. 68, 143-146 (2004). (Pubitemid 39093888)
19. A. K. Dunn, A. Devor, H. Bolay, M. L. Andermann, M. A. Moskowitz, A. M. Dale, and D. A. Boas, "Simultaneous imaging of total cerebral hemoglobin concentration, oxygenation, and blood flow during functional activation", Opt. Lett. 28, 28-30 (2003).
20. R. G. M. Kolkman, J. H. G. M. Klaessens, E. Hondebrink, J. C. W. Hopman, F. F. M. de Mul, W. Steenbergen, J. M. Thijssen, and T. G. van Leeuwen, "Photoacoustic determination of blood vessel diameter", Phys. Med. Biol. 49, 4745-4756 (2004). (Pubitemid 39433503)
21. X. Wang, G. Ku, M. A. Wegiel, D. J. Bornhop, G. Stoica, and L. V. Wang, "Noninvasive photoacoustic angiography of animal brains in vivo with near-infrared light and an optical contrast agent", Opt. Lett. 29, 730-732 (2004).
22. X. Wang, X. Xie, G. Ku, L. V. Wang, and G. Stoica, "Noninvasive imaging of hemoglobin concentration and oxygenation in the rat brain using high-resolution photoacoustic tomography", J. Biomed. Opt. 11, 024015 (2006).
23. C. K. Hitzenberger, P. Trost, P.-W. Lo, and Q. Zhou, "Three- dimensional imaging of the human retina by high-speed optical coherence tomography", Opt. Express 11, 2753-2761 (2003).
24. J. A. Izatt, M. D. Kulkarni, S. Yazdanfar, J. K. Barton, and A. J. Welch, "In vivo bidirectional color Doppler flow imaging of picoliter blood volumes using optical coherence tomography", Opt. Lett. 22, 1439-1441 (1997). (Pubitemid 127565229)
25. R. Michaely, A. H. Bachmann, M. L. Villiger, C. Blatter, T. Lasser, and R. A. Leitgeb, "Vectorial reconstruction of retinal blood flow in three dimensions measured with high resolution resonant Doppler Fourier domain optical coherence tomography", J. Biomed. Opt. 12, 041213 (2007).
26. D. J. Faber, E. G. Mick, M. C. G. Aalders, and T. G. van Leeuwen, "Toward assessment of blood oxygen saturation by spectroscopic optical coherence tomography", Opt. Lett. 30, 1015-1017 (2005). (Pubitemid 40749267)
27. D. J. Faber, E. G. Mik, M. C. G. Aalders, and T. G. van Leeuwen, "Light absorption of (oxy)-hemoglobin assessed by spectroscopic optical coherence tomography", Opt. Lett. 28, 1436-1438 (2003).
28. C.-W. Lu, C.-K. Lee, M.-T. Tsai, Y.-M. Wang, and C. C. Yang, "Measurement of the hemoglobin oxygen saturation level with spectroscopic spectral-domain optical coherence tomography", Opt. Lett. 33, 416-418 (2008). (Pubitemid 351431525)
29. L. Kagemann, G. Wollstein, M. Wojtkowski, H. Ishikawa, K. A. Townsend, M. L. Gabriele, V. J. Srinivasan, J. G. Fujimoto, and J. S. Schuman, "Spectral oximetry assessed with high-speed ultra-high resolution optical coherence tomography", J. Biomed. Opt. 12, 041212 (2007).
30. N. V. Iftimia, D. X. Hammer, C. E. Bigelow, D. I. Rosen, T. Ustun, A. A. Ferrante, D. Vu, and R. D. Ferguson, "Toward noninvasive measurement of blood hematocrit using spectral domain low coherence interferometry and retinal tracking", Opt. Express 14, 3377-3388 (2006).
31. A. Mariampillai, B. A. Standish, E. H. Moriyama, M. Khurana, N. R. Munce, M. K. K. Leung, J. Jiang, A. Cable, B. C. Wilson, A. Vitkin, and V. X. D. Yang, "Speckle variance detection of microvasculature using swept-source optical coherence tomography", Opt. Lett. 33, 1530-1532 (2008).
32. B. Styp-Rekowska, N. M. Disassa, B. Reglin, L. Ulm, H. Kuppe, T. W. Secomb, and A. R. Pries, "An imaging spectroscopy approach for measurement of oxygen saturation and hematocrit during intravital microscopy", Microcirculation (N. Y.) 14, 207-221 (2007). (Pubitemid 46552877)
33. H. Kobayashi and N. Takizawa, "Imaging of oxygen transfer among microvessels of rat cremaster muscle", Circulation 105, 1713-1719 (2002). (Pubitemid 34298617)
34. B. S. Sorg, M. E. Hardee, N. Agarwal, B. J. Moeller, and M. W. Dewhirst, "Spectral imaging facilitates visualization and measurements of unstable and abnormal microvascular oxygen transport in tumors", J. Biomed. Opt. 13, 014026 (2008).
35. B. S. Sorg, B. J. Moeller, O. Donovan, Y. Cao, and M. W. Dewhirst, "Hyperspectral imaging of hemoglobin saturation in tumor microvasculature and tumor hypoxia development", J. Biomed. Opt. 10, 044004 (2005).
36. M. C. Skala, A. Fontanella, H. Hendargo, M. W. Dewhirst, and J. A. Izatt, "Combined hyperspectral and spectral domain optical coherence tomography microscope for noninvasive hemodynamic imaging", Opt. Lett. 34, 289-291 (2009).
37. R. D. Shonat, E. S. Wachman, W.-H. Niu, A. P. Koretsky, and D. L. Farkas, "Near-simultaneous hemoglobin saturation and oxygen tension maps in mouse brain using an AOTF microscope", Biophys. J. 73, 1223-1231 (1997). (Pubitemid 27360712)
38. S. O. Park, Y. J. Lee, T. Seki, K.-H. Hong, N. Fliess, Z. Jiang, A. Park, X. Wu, V. Kaartinen, B. L. Roman, and S. P. Oh, "ALK5-and TGFBR2-independent role of ALK1 in the pathogenesis of hereditary hemorrhagic telangiectasia type 2", Blood 111, 633-642 (2008).
39. J. L. Unthank, J. M. Lash, J. C. Nixon, R. A. Sidner, and H. G. Bohlen, "Evaluation of carbocyanine-labeled erythrocytes for microvascular measurements", Microvasc. Res. 45, 193-210 (1993).
40. C. deDeugd, M. Wankhede, and B. S. Sorg, "Multimodal optical imaging of microvessel network convective oxygen transport dynamics", Appl. Opt. 48, D187-D197 (2009).
41. A. J. Ferreira and M. K. Raizada, "Genomic and proteomic approaches for targeting of angiotensin-converting enzyme2 for cardiovascular diseases", Curr. Opin. Cardiol. 23, 364-369 (2008). (Pubitemid 351787102)
42. R. A. Santos, A. J. Ferreira, E. Simões, and A. C. Silva, "Recent advances in the angiotensin-converting enzyme 2-angiotensin (1-7) - Mas axis", Exp. Physiol. 93, 519-527 (2008). (Pubitemid 351595060)
43. T. Katayama, Y. Ikeda, M. Handa, T. Tamatani, S. Sakamoto, M. Ito, Y. Ishimura, and M. Suematsu, "Immunoneutralization of glycoprotein Iba attenuates endotoxin-induced interactions of platelets and leukocytes with rat venular endothelium in vivo", Circ. Res. 86, 1031-1037 (2000). (Pubitemid 30367861)
44. P. Vaupel, F. Kallinowski, and P. Okunieff, "Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review", Cancer Res. 49, 6449-6465 (1989). (Pubitemid 20008770)
45. J. Folkman, "Tumor angiogenesis: therapeutic implications", N. Engl. J. Med. 285, 1182-1186 (1971).
46. R. G. Bristow and R. P. Hill, "Hypoxia, DNA repair and genetic instability", Nat. Rev. Cancer 8, 180-192 (2008).
47. R. E. Durand and C. Aquino-Parsons, "Non-constant tumour blood flow-implications for therapy", Acta Oncol. 40, 862-869 (2001). (Pubitemid 34081666)
48. R. E. Durand and C. Aquino-Parsons, "Clinical relevance of intermittent tumour blood flow", Acta Oncol. 40, 929-936 (2001). (Pubitemid 34098479)
49. E. K. Rofstad, K. Galappathi, B. Mathiesen, and E.-B. M. Ruud, "Fluctuating and diffusion-limited hypoxia in hypoxia-induced metastasis", Clin. Cancer Res. 13, 1971-1978 (2007). (Pubitemid 46649862)
50. K. G. Brurberg, J.-V. Gaustad, C. S. Mollatt, and E. K. Rofstad, "Temporal heterogeneity in blood supply in human tumor xenografts", Neoplasia 10, 727-735 (2008). (Pubitemid 351883889)
51. J.-V. Gaustad, T. G. Simonsen, K. G. Brurberg, E. M. Huuse, and E. K. Rofstad, "Blood supply in melanoma xenografts is governed by the morphology of the supplying arteries", Neoplasia 11, 277-285 (2009).
52. M. E. Hardee, M. W. Dewhirst, N. Agarwal, and B. S. Sorg, "Novel imaging provides new insights into mechanisms of oxygen transport in tumors", Curr. Mol. Med. 9, 435-441 (2009).
53. K. Konner, "The initial creation of native arteriovenous fistulas: surgical aspects and their impact on the practice of nephrology", Semin. Dial. 16, 291-298 (2003). (Pubitemid 37340257)
54. R. K. Jain, "Determinents of tumor blood flow: a review", Cancer Res. 48, 2641-2658 (1988).
55. J. Widdicombe, "Microvascular anatomy of the nose", Allergy 52(Suppl. 1), 7-11 (1997). (Pubitemid 27444750)
56. A. Zakrzewicz, T. W. Secomb, and A. R. Pries, "Angioadaptation: keeping the vascular system in shape", News Physiol. Sci. 17, 197-201 (2002).
57. A. A. Sharathkumar and A. Shapiro, "Hereditary haemorrhagic telangiectasia", Haemophilia 14, 1269-1280 (2008).
58. J. Berg, M. Porteous, D. Reinhardt, C. Gallione, S. Holloway, T. Umasunthar, A. Lux, W. McKinnon, D. Marchuk, and A. Guttmacher, "Hereditary haemorrhagic telangiectasia: a questionnaire based study to delineate the different phenotypes caused by endoglin and ALK1 mutations", J. Med. Genet. 40, 585-590 (2003). (Pubitemid 37046911)
59. H. Sadick, M. Sadick, K. Götte, R. Naim, F. Riedel, G. Bran, and K. Hörmann, "Hereditary hemorrhagic telangiectasia: an update on clinical manifestations and diagnostic measures", Wien. Klin. Wochenschr. 118, 72-80 (2006).
60. A. C. Guyton, Textbook of Medical Physiology, W. B. Saunders Company, Philadelphia (1991).
61. D. J. Fitzgerald, "Vascular biology of thrombosis: the role of plateletvessel wall adhesion", Neurology 57(Suppl. 2), S1-S4 (2001). (Pubitemid 32831454)
62. P. A. Kyrle and S. Eichinger, "Deep vein thrombosis", Lancet 365, 1163-1174 (2005). (Pubitemid 40417567)
63. R. A. Fraga-Silva, B. S. Sorg, M. Wankhede, C. deDeugd, J. Y. Jun, M. B. Baker, Y. Li, R. K. Castellano, M. J. Katovich, M. K. Raizada, and A. J. Ferreira, "ACE2 activation promotes anti-thrombotic activity", Mol. Med. (in press).
64. M. W. Dewhirst, "Intermittent hypoxia furthers the rationale for hypoxia-inducible factor-1 targeting", Cancer Res. 67, 854-855 (2007).
65. J. Lanzen, R. D. Braun, B. Klitzman, D. Brizel, T. W. Secomb, and M. W. Dewhirst, "Direct demonstration of instabilities in oxygen concentrations within the extravascular compartment of an experimental tumor", Cancer Res. 66, 2219-2223 (2006).
66. A. D. Estrada, A. Ponticorvo, T. N. Ford, and A. K. Dunn, "Microvascular oxygen quantification using two-photon microscopy", Opt. Lett. 33, 1038-1040 (2008).
67. J. D. Briers, "Laser Doppler, speckle and related techniques for blood perfusion mapping and imaging", Physiol. Meas 22, R35-R66 (2001). (Pubitemid 33104651)
68. Y.-C. Yu-Chih Huang, T. L. Ringold, J. S. Nelson, and B. Choi, "Noninvasive blood flow imaging for real-time feedback during laser therapy of port wine stain birthmarks", Lasers Surg. Med. 40, 167-173 (2008). (Pubitemid 351500142)
69. Y. Wang, B. A. Bower, J. A. Izatt, O. Tan, and D. Huang, "In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography", J. Biomed. Opt. 12, 041215 (2007).
70. M. Sivaramakrishnan, K. Maslov, H. F. Zhang, G. Stoica, and L. V. Wang, "Limitations of quantitative photoacoustic measurements of blood oxygenation in small vessels", Phys. Med. Biol. 52, 1349-1361 (2007). (Pubitemid 46646392)
71. H. Kerger, G. Groth, K. Kalenka, P. Vajkoczy, A. G. Tsai, and M. Intaglietta, "pO2 measurements by phosphorescence quenching: characteristics and applications of an automated system", Microvasc. Res. 65, 32-38 (2003). (Pubitemid 36263288)
72. T. Binzoni, A. Vogel, A. H. Gandjbakhche, and R. Marchesini, "Detection limits of multi-spectral optical imaging under the skin surface", Phys. Med. Biol. 53, 617-636 (2008). (Pubitemid 351496209)
73. S. Shan, B. S. Sorg, and M. W. Dewhirst, "A novel rodent mammary window of orthotopic breast cancer for intravital microscopy", Microvasc. Res. 65, 109-117 (2003). (Pubitemid 36398645)
74. J. C. Ramella-Roman, S. A. Mathews, H. Kandimalla, A. Nabili, D. D. Duncan, S. A. D'Anna, S. M. Shah, and Q. D. Nguyen, "Measurement of oxygen saturation in the retina with a spectroscopic sensitive multi aperture camera", Opt. Express 16, 6170-6182 (2008). (Pubitemid 351623330)
75. W. R. Johnson, D. W. Wilson, W. Fink, M. Humayun, and G. Bearman, "Snapshot hyperspectral imaging in ophthalmology", J. Biomed. Opt. 12, 014036 (2007).
76. M. E. Gehm, R. John, D. J. Brady, R. M. Willett, and T. J. Schulz, "Single-shot compressive spectral imaging with a dual-disperser architecture", Opt. Express 15, 14013-14027 (2007). (Pubitemid 47608612)
77. A. A. Wagadarikar, N. P. Pitsianis, X. Sun, and D. J. Brady, "Video rate spectral imaging using a coded aperture snapshot spectral imager", Opt. Express 17, 6368-6388 (2009).
78. B. R. Duling and R. M. Berne, "Longitudinal gradients in periarteriolar oxygen tension", Circ. Res. 27, 669-678 (1970).
79. B. R. Duling, "Microvascular responses to alterations in oxygen tension", Circ. Res. 31, 481-489 (1972).
80. R. D. Shonat and P. C. Johnson, "Oxygen tension gradients and heterogeneity in venous microcirculation: a phosphorescence quenching study", Am. J. Physiol. Heart Circ. Physiol. 272, H2233-H2240 (1997).
81. M. W. Dewhirst, Y. Cao, and B. J. Moeller, "Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response", Nat. Rev. Cancer 8, 425-437 (2008). (Pubitemid 351744964)
82. L. I. Cardenas-Navia, D. Mace, R. A. Richardson, D. F. Wilson, S. Shan, and M. W. Dewhirst, "The pervasive presence of fluctuating oxygenation in tumors", Cancer Res. 68, 5812-5819 (2008).
83. P. Martinive, F. Defresne, C. Bouzin, J. Saliez, F. Lair, V. Grégoire, C. Michiels, C. Dessy, and O. Feron, "Preconditioning of the tumor vasculature and tumor cells by intermittent hypoxia: implications for anticancer therapies", Cancer Res. 66, 11736-11744 (2006). (Pubitemid 46094185)
84. K. S. Øye, G. Gulati, B. A. Graff, J.-V. Gaustad, K. G. Brurberg, and E. K. Rofstad, "A novel method for mapping the heterogeneity in blood supply to normal and malignant tissues in the mouse dorsal window chamber", Microvasc. Res. 75, 179-187 (2008). (Pubitemid 351249858)
85. I. M. Braverman, A. Keh, and B. S. Jacobson, "Ultrastructure and three-dimensional organization of the telangiectases of hereditary hemorrhagic telangiectasia", J. Invest. Dermatol. 95, 422-427 (1990). (Pubitemid 20331987)
86. P. A. Murphy, M. T. Y. Lam, X. Wu, T. N. Kim, S. M. Vartanian, A. W. Bollen, T. R. Carlson, and R. A. Wang, "Endothelial Notch4 signaling induces hallmarks of brain arteriovenous malformations in mice", Proc. Natl. Acad. Sci. U. S. A. 105, 10901-10906 (2008).
87. S. O. Park, M. Wankhede, Y. J. Lee, E.-J. Choi, N. Fliess, S. Choe, S.-H. Oh, G. Walter, M. K. Raizada, B. S. Sorg, and S. P. Oh, "Realtime imaging of de novo arteriovenous malformation in a mouse model of hereditary hemorrhagic telangiectasia", J. Clin. Invest. 119, 3487-3496 (2009).
88. S. Willoughby, A. Holmes, and J. Loscalzo, "Platelets and cardiovascular disease", Eur. J. Cardiovasc. Nurs. 1, 273-288 (2002). (Pubitemid 36857068)
89. R. N. Pittman, "Oxygen transport and exchange in the microcirculation", Microcirculation (NY.) 12, 59-70 (2005). (Pubitemid 40450618)
90. T. W. Secomb, R. Hsu, E. Y. H. Park, and M. W. Dewhirst, "Green's function methods for analysis of oxygen delivery to tissue by microvascular networks", Ann. Biomed. Eng. 32, 1519-1529 (2004). (Pubitemid 40044498)