Ultrasound in Medicine and Biology
Volume 33, Issue 4 , Pages 549-560 , April 2007

Methodology for Quantifying Interactions Between Perfusion Evaluated by DCE-US and Hypoxia Throughout Tumor Growth

  • Nicolas Elie

      Affiliations

    • UPRES-EA 4040: Imagerie Fonctionnelle de la Microvascularisation et de la Perfusion Tumorales, Gustave Roussy Institue, Villejuif
    • ,
  • Alexandre Kaliski

      Affiliations

    • UPRES-EA 4040: Imagerie Fonctionnelle de la Microvascularisation et de la Perfusion Tumorales, Gustave Roussy Institue, Villejuif
    • ,
  • Pierre Péronneau

      Affiliations

    • UPRES-EA 4040: Imagerie Fonctionnelle de la Microvascularisation et de la Perfusion Tumorales, Gustave Roussy Institue, Villejuif
    • ,
  • Paule Opolon

      Affiliations

    • Laboratoire de Vectorologie et de Transfert de genes, Gustave Roussy Institue, Villejuif, France
    • ,
  • Alain Roche

      Affiliations

    • UPRES-EA 4040: Imagerie Fonctionnelle de la Microvascularisation et de la Perfusion Tumorales, Gustave Roussy Institue, Villejuif
    • Departement d’Imagerie, Gustave Roussy Institue, Villejuif, France
    • ,
  • Nathalie Lassau

      Affiliations

    • UPRES-EA 4040: Imagerie Fonctionnelle de la Microvascularisation et de la Perfusion Tumorales, Gustave Roussy Institue, Villejuif
    • Departement d’Imagerie, Gustave Roussy Institue, Villejuif, France
    • Corresponding Author InformationAddress correspondence to: Nathalie Lassau, MD, PhD, UPRES-EA 4040: “Imagerie fonctionnelle de la microvascularisation et de la perfusion tumorales,” Institut Gustave Roussy, 94800 Villejuif, France.

Received 1 June 2006 ,Revised 15 September 2006 ,Accepted 26 September 2006.

References 

  1. Adam MF, Dorie MJ, Brown JM. Oxygen tension measurements of tumors growing in mice. Int J Radiat Oncol Biol Phys. 1999;45:171–180
  2. Albrecht T, Blomley MJ, Cosgrove DO, et al. Non-invasive diagnosis of hepatic cirrhosis by transit-time analysis of an ultrasound contrast agent. Lancet. 1999;353:1579–1583
  3. Baudelet C, Gallez B. Effect of anesthesia on the signal intensity in tumors using BOLD-MRI: Comparison with flow measurements by Laser Doppler flowmetry and oxygen measurements by luminescence-based probes. Magn Reson Imaging. 2004;22:905–912
  4. Bhagavatheeshwaran G, Shi WT, Forsberg F, Shankar PM. Subharmonic signal generation from contrast agents in simulated neovessels. Ultrasound Med Biol. 2004;30:199–203
  5. Braun RD, Lanzen JL, Snyder SA, Dewhirst MW. Comparison of tumor and normal tissue oxygen tension measurements using OxyLite or microelectrodes in rodents. Am J Physiol Heart Circ Physiol. 2001;280:H2533–H2544
  6. Bruce M, Averkiou M, Tiemann K, Lohmaier S, Powers J, Beach K. Vascular flow and perfusion imaging with ultrasound contrast agents. Ultrasound Med Biol. 2004;30:735–743
  7. Brurberg KG, Graff BA, Olsen DR, Rofstad EK. Tumor-line specific pO(2) fluctuations in human melanoma xenografts. Int J Radiat Oncol Biol Phys. 2004;58:403–409
  8. Brurberg KG, Graff BA, Rofstad EK. Temporal heterogeneity in oxygen tension in human melanoma xenografts. Br J Cancer. 2003;89:350–356
  9. Bussink J, Kaanders JH, Strik AM, Vojnovic B, van Der Kogel AJ. Optical sensor-based oxygen tension measurements correspond with hypoxia marker binding in three human tumor xenograft lines. Radiat Res. 2000;154:547–555
  10. Carmeliet P. Angiogenesis in health and disease. Nat Med. 2003;9:653–660
  11. Choyke PL, Chen CA, Cheng WF, et al. Contrast agents for imaging tumor angiogenesis: Is bigger better?. Radiology. 2005;235:1–2
  12. De Jaeger K, Merlo FM, Kavanagh MC, Fyles AW, Hedley D, Hill RP. Heterogeneity of tumor oxygenation: relationship to tumor necrosis, tumor size, and metastasis. Int J Radiat Oncol Biol Phys. 1998;42:717–721
  13. Dewhirst MW, Klitzman B, Braun RD, Brizel DM, Haroon ZA, Secomb TW. Review of methods used to study oxygen transport at the microcirculatory level. Int J Cancer. 2000;90:237–255
  14. Eberhard A, Kahlert S, Goede V, Hemmerlein B, Plate KH, Augustin HG. Heterogeneity of angiogenesis and blood vessel maturation in human tumors: Implications for antiangiogenic tumor therapies. Cancer Res. 2000;60:1388–1393
  15. Elie N, Plancoulaine B, Signolle JP, Herlin P. A simple way of quantifying immunostained cell nuclei on the whole histologic section. Cytometry A. 2003;56:37–45
  16. Evans SM, Judy KD, Dunphy I, et al. Comparative measurements of hypoxia in human brain tumors using needle electrodes and EF5 binding. Cancer Res. 2004;64:1886–1892
  17. Fleischer AC, Niermann KJ, Donnelly EF, et al. Sonographic depiction of microvessel perfusion: principles and potential. J Ultrasound Med. 2004;23:1499–1506
  18. Frinking PJ, Bouakaz A, Kirkhorn J, Ten Cate FJ, de Jong N. Ultrasound contrast imaging: current and new potential methods. Ultrasound Med Biol. 2000;26:965–975
  19. Gabbiani G. The myofibroblast in wound healing and fibrocontractive diseases. J Pathol. 2003;200:500–503
  20. Gee MS, Saunders HM, Lee JC, et al. Doppler ultrasound imaging detects changes in tumor perfusion during antivascular therapy associated with vascular anatomic alterations. Cancer Res. 2001;61:2974–2982
  21. Griffiths JR, Robinson SP. The OxyLite: A fibre-optic oxygen sensor. Br J Radiol. 1999;72:627–630
  22. Hagendoorn J, Tong R, Fukumura D, et al. Onset of abnormal blood and lymphatic vessel function and interstitial hypertension in early stages of carcinogenesis. Cancer Res. 2006;66:3360–3364
  23. Heldin CH, Rubin K, Pietras K, Ostman A. High interstitial fluid pressure—An obstacle in cancer therapy. Nat Rev Cancer. 2004;4:806–813
  24. Hoskin PJ, Sibtain A, Daley FM, Wilson GD. GLUT1 and CAIX as intrinsic markers of hypoxia in bladder cancer: Relationship with vascularity and proliferation as predictors of outcome of ARCON. Br J Cancer. 2003;89:1290–1297
  25. Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003;9:685–693
  26. Jain RK. Normalization of tumor vasculature: An emerging concept in antiangiogenic therapy. Science. 2005;307:58–62
  27. Jordan BF, Sonveaux P, Feron O, Gregoire V, Beghein N, Gallez B. Nitric oxide-mediated increase in tumor blood flow and oxygenation of tumors implanted in muscles stimulated by electric pulses. Int J Radiat Oncol Biol Phys. 2003;55:1066–1073
  28. Lassau N, Koscielny S, Opolon P, et al. Evaluation of contrast-enhanced color Doppler ultrasound for the quantification of angiogenesis in vivo. Invest Radiol. 2001;36:50–55
  29. Lassau N, Lamuraglia M, Vanel D, et al. Doppler US with perfusion software and contrast medium injection in the early evaluation of isolated limb perfusion of limb sarcomas: prospective study of 49 cases. Ann Oncol. 2005;16:1054–1060
  30. Lassau N, Mercier S, Koscielny S, et al. Prognostic value of high-frequency sonography and color Doppler sonography for the preoperative assessment of melanomas. AJR Am J Roentgenol. 1999;172:457–461
  31. Li J, Dong B, Yu X, Wang X, Li C. Grey-scale contrast enhancement in rabbit liver with SonoVue at different doses. Ultrasound Med Biol. 2005;31:185–190
  32. Li J, Dong BW, Yu XL, Wang XH, Li CF. Time-intensity-based quantification of vascularity with single-level dynamic contrast-enhanced ultrasonography: A pilot animal study. J Ultrasound Med. 2005;24:975–983
  33. Menon C, Polin GM, Prabakaran I, et al. An integrated approach to measuring tumor oxygen status using human melanoma xenografts as a model. Cancer Res. 2003;63:7232–7240
  34. Miller JC, Pien HH, Sahani D, Sorensen AG, Thrall JH. Imaging angiogenesis: Applications and potential for drug development. J Natl Cancer Inst. 2005;97:172–187
  35. Milosevic M, Fyles A, Hedley D, Hill R. The human tumor microenvironment: Invasive (needle) measurement of oxygen and interstitial fluid pressure. Semin Radiat Oncol. 2004;14:249–258
  36. Mueller MM, Fusenig NE. Friends or foes—Bipolar effects of the tumour stroma in cancer. Nat Rev Cancer. 2004;4:839–849
  37. Niermann KJ, Fleischer AC, Donnelly EF, Schueneman AJ, Geng L, Hallahan DE. Sonographic depiction of changes of tumor vascularity in response to various therapies. Ultrasound Q. 2005;21:61–67quiz 149, 153–144
  38. Nozue M, Lee I, Yuan F, et al. Interlaboratory variation in oxygen tension measurement by Eppendorf “Histograph” and comparison with hypoxic marker. J Surg Oncol. 1997;66:30–38
  39. Olive PL, Aquino-Parsons C. Measurement of tumor hypoxia using single-cell methods. Semin Radiat Oncol. 2004;14:241–248
  40. Padera TP, Stoll BR, Tooredman JB, Capen D, di Tomaso E, Jain RK. Pathology: Cancer cells compress intratumour vessels. Nature. 2004;427:695
  41. Parker C, Milosevic M, Toi A, et al. Polarographic electrode study of tumor oxygenation in clinically localized prostate cancer. Int J Radiat Oncol Biol Phys. 2004;58:750–757
  42. Roth DM, Swaney JS, Dalton ND, Gilpin EA, Ross J. Impact of anesthesia on cardiac function during echocardiography in mice. Am J Physiol Heart Circ Physiol. 2002;282:H2134–H2140
  43. Rouffiac V, Bouquet C, Lassau N, et al. Validation of a new method for quantifying in vivo murine tumor necrosis by sonography. Invest Radiol. 2004;39:350–356
  44. Scholbach T, Scholbach J, Krombach GA, Gagel B, Maneschi P, Di Martino E. New method of dynamic color Doppler signal quantification in metastatic lymph nodes compared to direct polarographic measurements of tissue oxygenation. Int J Cancer. 2005;114:957–962
  45. Seddon BM, Honess DJ, Vojnovic B, Tozer GM, Workman P. Measurement of tumor oxygenation: In vivo comparison of a luminescence fiber-optic sensor and a polarographic electrode in the p22 tumor. Radiat Res. 2001;155:837–846
  46. Shannon AM, Bouchier-Hayes DJ, Condron CM, Toomey D. Tumour hypoxia, chemotherapeutic resistance and hypoxia-related therapies. Cancer Treat Rev. 2003;29:297–307
  47. Shi WT, Forsberg F, Bautista R, Vecchio C, Bernardi R, Goldberg BB. Image enhancement by acoustic conditioning of ultrasound contrast agents. Ultrasound Med Biol. 2004;30:191–198
  48. Thijssen JM, de Korte CL. Modeling ultrasound contrast measurement of blood flow and perfusion in biological tissue. Ultrasound Med Biol. 2005;31:279–285
  49. Tufto I, Rofstad EK. Interstitial fluid pressure, fraction of necrotic tumor tissue, and tumor cell density in human melanoma xenografts. Acta Oncol. 1998;37:291–297
  50. Vaupel P. Tumor microenvironmental physiology and its implications for radiation oncology. Semin Radiat Oncol. 2004;14:198–206
  51. Veltmann C, Lohmaier S, Schlosser T, et al. On the design of a capillary flow phantom for the evaluation of ultrasound contrast agents at very low flow velocities. Ultrasound Med Biol. 2002;28:625–634
  52. Vujaskovic Z, Rosen EL, Blackwell KL, et al. Ultrasound guided pO2 measurement of breast cancer reoxygenation after neoadjuvant chemotherapy and hyperthermia treatment. Int J Hyperthermia. 2003;19:498–506
  53. Yeh KA, Biade S, Lanciano RM, et al. Polarographic needle electrode measurements of oxygen in rat prostate carcinomas: Accuracy and reproducibility. Int J Radiat Oncol Biol Phys. 1995;33:111–118

PII: S0301-5629(06)01864-3

doi: 10.1016/j.ultrasmedbio.2006.09.011

Ultrasound in Medicine and Biology
Volume 33, Issue 4 , Pages 549-560 , April 2007

Article Tools

* Image Usage & Resolution