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[Cancer Research 56, 941-943, March 1, 1996]
© 1996 American Association for Cancer Research
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Tumor Oxygenation Predicts for the Likelihood of Distant Metastases in Human Soft Tissue Sarcoma1

David M. Brizel2, Sean P. Scully, John M. Harrelson, Lester J. Layfield, Joseph M. Bean, Leonard R. Prosnitz and Mark W. Dewhirst

Departments of Radiation Oncology [D. M., B., J. M. B., L. R. P., M. W. D.] and Pathology [L. J. L.] and Division of Orthopedics, Department of Surgery [S. P. S., J. M. H.], Duke University Comprehensive Cancer Center, Durham, North Carolina 27710

This study was performed to explore the relationship between tumor oxygenation and treatment outcome in human soft tissue sarcoma. Twenty-two patients with nonmetastatic, high-grade, soft tissue sarcomas underwent preoperative irradiation and hyperthermia and pretreatment measurement of tumor oxygenation. The 18-month actuarial disease-free survival was 70% for patients with tumor median oxygen pressure (pO2) values of >10 mm Hg but only 35% for those with median pO2 values of < 10 mm Hg (P = 0.01). There were eight treatment failures; the first site of recurrence was lung in all patients. Median pO2 was 7.5 mm Hg for metastasizing tumors versus 20 mm Hg for nonmetastasizing tumors (P = 0.03). Potential mechanisms and implications for clinical trial design are discussed.

1 This work was supported by NIH Grant CA42745.

2 To whom requests for reprints should be addressed, at Department of Radiation Oncology, Box 3085, Duke University Medical Center, Durham, NC 27710. Phone: (919) 660-2119; Fax: (919) 684-3953; E-mail: brizel@radonc.duke.edu.

Received 12/ 1/95. Accepted 1/17/96.




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T. Lofstedt, A. Jogi, M. Sigvardsson, K. Gradin, L. Poellinger, S. Pahlman, and H. Axelson
Induction of ID2 Expression by Hypoxia-inducible Factor-1: A ROLE IN DEDIFFERENTIATION OF HYPOXIC NEUROBLASTOMA CELLS
J. Biol. Chem., September 17, 2004; 279(38): 39223 - 39231.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
Q.-T. Le, J. McCoy, S. Williamson, J. Ryu, L. E. Gaspar, M. J. Edelman, S. R. Dakhil, S. D. Sides, J. J. Crowley, and D. R. Gandara
Phase I Study of Tirapazamine Plus Cisplatin/Etoposide and Concurrent Thoracic Radiotherapy in Limited-Stage Small Cell Lung Cancer (S0004): A Southwest Oncology Group Study
Clin. Cancer Res., August 15, 2004; 10(16): 5418 - 5424.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. Okami, D. M. Simeone, and C. D. Logsdon
Silencing of the Hypoxia-Inducible Cell Death Protein BNIP3 in Pancreatic Cancer
Cancer Res., August 1, 2004; 64(15): 5338 - 5346.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
E. L. Jones, L. R. Prosnitz, M. W. Dewhirst, P. K. Marcom, P. H. Hardenbergh, L. B. Marks, D. M. Brizel, and Z. Vujaskovic
Thermochemoradiotherapy Improves Oxygenation in Locally Advanced Breast Cancer
Clin. Cancer Res., July 1, 2004; 10(13): 4287 - 4293.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
K. Maseide, R. A. Kandel, R. S. Bell, C. N. Catton, B. O'Sullivan, J. S. Wunder, M. Pintilie, D. Hedley, and R. P. Hill
Carbonic Anhydrase IX as a Marker for Poor Prognosis in Soft Tissue Sarcoma
Clin. Cancer Res., July 1, 2004; 10(13): 4464 - 4471.
[Abstract] [Full Text] [PDF]

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 Evid Based Complement Alternat MedHome page
B. Clavo, J. L. Perez, L. Lopez, G. Suarez, M. Lloret, V. Rodriguez, D. Macias, M. Santana, M. A. Hernandez, R. Martin-Oliva, et al.
Ozone Therapy for Tumor Oxygenation: a Pilot Study
Evid. Based Complement. Altern. Med., June 1, 2004; 1(1): 93 - 98.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Regul. Integr. Comp. Physiol.Home page
G. Hopfl, O. Ogunshola, and M. Gassmann
HIFs and tumors--causes and consequences
Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2004; 286(4): R608 - R623.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. A. Cairns and R. P. Hill
Acute Hypoxia Enhances Spontaneous Lymph Node Metastasis in an Orthotopic Murine Model of Human Cervical Carcinoma
Cancer Res., March 15, 2004; 64(6): 2054 - 2061.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
S. M. Evans, K. D. Judy, I. Dunphy, W. T. Jenkins, P. T. Nelson, R. Collins, E. P. Wileyto, K. Jenkins, S. M. Hahn, C. W. Stevens, et al.
Comparative Measurements of Hypoxia in Human Brain Tumors Using Needle Electrodes and EF5 Binding
Cancer Res., March 1, 2004; 64(5): 1886 - 1892.
[Abstract] [Full Text] [PDF]

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 Molecular Cancer TherapeuticsHome page
S. Welsh, R. Williams, L. Kirkpatrick, G. Paine-Murrieta, and G. Powis
Antitumor activity and pharmacodynamic properties of PX-478, an inhibitor of hypoxia-inducible factor-1{alpha}
Mol. Cancer Ther., March 1, 2004; 3(3): 233 - 244.
[Abstract] [Full Text]

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 Am. J. Pathol.Home page
D. Hedley, M. Pintilie, J. Woo, T. Nicklee, A. Morrison, D. Birle, A. Fyles, M. Milosevic, and R. Hill
Up-Regulation of the Redox Mediators Thioredoxin and Apurinic/Apyrimidinic Excision (APE)/Ref-1 in Hypoxic Microregions of Invasive Cervical Carcinomas, Mapped Using Multispectral, Wide-Field Fluorescence Image Analysis
Am. J. Pathol., February 1, 2004; 164(2): 557 - 565.
[Abstract] [Full Text] [PDF]

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 Recent Prog Horm ResHome page
M. L. Wahl, T. L. Moser, and S. V. Pizzo
Angiostatin and Anti-angiogenic Therapy in Human Disease
Recent Prog. Horm. Res., January 1, 2004; 59(1): 73 - 104.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
C. Delmas, D. End, P. Rochaix, G. Favre, C. Toulas, and E. Cohen-Jonathan
The Farnesyltransferase Inhibitor R115777 Reduces Hypoxia and Matrix Metalloproteinase 2 Expression in Human Glioma Xenograft
Clin. Cancer Res., December 1, 2003; 9(16): 6062 - 6068.
[Abstract] [Full Text] [PDF]

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 Br. J. Radiol.Home page
N Raghunand, R A Gatenby, and R J Gillies
Microenvironmental and cellular consequences of altered blood flow in tumours
Br. J. Radiol., December 1, 2003; 76(suppl_1): S11 - S22.
[Abstract] [Full Text] [PDF]

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 Br. J. Radiol.Home page
B M Seddon and P Workman
The role of functional and molecular imaging in cancer drug discovery and development
Br. J. Radiol., December 1, 2003; 76(suppl_2): S128 - S138.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
K. L. Blackwell, J. P. Kirkpatrick, S. A. Snyder, G. Broadwater, F. Farrell, L. Jolliffe, D. M. Brizel, and M. W. Dewhirst
Human Recombinant Erythropoietin Significantly Improves Tumor Oxygenation Independent of Its Effects on Hemoglobin
Cancer Res., October 1, 2003; 63(19): 6162 - 6165.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
P. N. Lara Jr., P. Frankel, P. C. Mack, P. H. Gumerlock, I. Galvin, C. L. Martel, J. Longmate, J. H. Doroshow, H. J. Lenz, D. H. M. Lau, et al.
Tirapazamine Plus Carboplatin and Paclitaxel in Advanced Malignant Solid Tumors: A California Cancer Consortium Phase I and Molecular Correlative Study
Clin. Cancer Res., October 1, 2003; 9(12): 4356 - 4362.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
V. T. Mihaylova, R. S. Bindra, J. Yuan, D. Campisi, L. Narayanan, R. Jensen, F. Giordano, R. S. Johnson, S. Rockwell, and P. M. Glazer
Decreased Expression of the DNA Mismatch Repair Gene Mlh1 under Hypoxic Stress in Mammalian Cells
Mol. Cell. Biol., May 1, 2003; 23(9): 3265 - 3273.
[Abstract] [Full Text] [PDF]

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 FASEB J.Home page
F. HEDBORG, E. ULLERAS, L. GRIMELIUS, E. WASSBERG, P. H MAXWELL, B. HERO, F. BERTHOLD, F. SCHILLING, D. HARMS, B. SANDSTEDT, et al.
Evidence for hypoxia-induced neuronal-to-chromaffin metaplasia in neuroblastoma
FASEB J, April 1, 2003; 17(6): 598 - 609.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
K. Helczynska, A. Kronblad, A. Jogi, E. Nilsson, S. Beckman, G. Landberg, and S. Pahlman
Hypoxia Promotes a Dedifferentiated Phenotype in Ductal Breast Carcinoma in Situ
Cancer Res., April 1, 2003; 63(7): 1441 - 1444.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
J. H. A. M. Kaanders, K. I. E. M. Wijffels, H. A. M. Marres, A. S. E. Ljungkvist, L. A. M. Pop, F. J. A. van den Hoogen, P. C. M. de Wilde, J. Bussink, J. A. Raleigh, and A. J. van der Kogel
Pimonidazole Binding and Tumor Vascularity Predict for Treatment Outcome in Head and Neck Cancer
Cancer Res., December 1, 2002; 62(23): 7066 - 7074.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
C. C. Hudson, M. Liu, G. G. Chiang, D. M. Otterness, D. C. Loomis, F. Kaper, A. J. Giaccia, and R. T. Abraham
Regulation of Hypoxia-Inducible Factor 1{alpha} Expression and Function by the Mammalian Target of Rapamycin
Mol. Cell. Biol., October 15, 2002; 22(20): 7004 - 7014.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
E. P. Hui, A. T. C. Chan, F. Pezzella, H. Turley, K.-F. To, T. C. W. Poon, B. Zee, F. Mo, P. M. L. Teo, D. P. Huang, et al.
Coexpression of Hypoxia-inducible Factors 1{alpha} and 2{alpha}, Carbonic Anhydrase IX, and Vascular Endothelial Growth Factor in Nasopharyngeal Carcinoma and Relationship to Survival
Clin. Cancer Res., August 1, 2002; 8(8): 2595 - 2604.
[Abstract] [Full Text] [PDF]

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 Clin. Cancer Res.Home page
B. M. Seddon, R. J. Maxwell, D. J. Honess, R. Grimshaw, F. Raynaud, G. M. Tozer, and P. Workman
Validation of the Fluorinated 2-Nitroimidazole SR-4554 as a Noninvasive Hypoxia Marker Detected by Magnetic Resonance Spectroscopy
Clin. Cancer Res., July 1, 2002; 8(7): 2323 - 2335.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
A. Jogi, I. Ora, H. Nilsson, A. Lindeheim, Y. Makino, L. Poellinger, H. Axelson, and S. Pahlman
Hypoxia alters gene expression in human neuroblastoma cells toward an immature and neural crest-like phenotype
PNAS, May 14, 2002; 99(10): 7021 - 7026.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
E. K. Rofstad, H. Rasmussen, K. Galappathi, B. Mathiesen, K. Nilsen, and B. A. Graff
Hypoxia Promotes Lymph Node Metastasis in Human Melanoma Xenografts by Up-Regulating the Urokinase-Type Plasminogen Activator Receptor
Cancer Res., March 1, 2002; 62(6): 1847 - 1853.
[Abstract] [Full Text] [PDF]

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 JCOHome page
A. Fyles, M. Milosevic, D. Hedley, M. Pintilie, W. Levin, L. Manchul, and R. P. Hill
Tumor Hypoxia Has Independent Predictor Impact Only in Patients With Node-Negative Cervix Cancer
J. Clin. Oncol., February 1, 2002; 20(3): 680 - 687.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
H. Nishi, K. H. Nishi, and A. C. Johnson
Early Growth Response-1 Gene Mediates Up-Regulation of Epidermal Growth Factor Receptor Expression during Hypoxia
Cancer Res., February 1, 2002; 62(3): 827 - 834.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
R. A. Cairns, T. Kalliomaki, and R. P. Hill
Acute (Cyclic) Hypoxia Enhances Spontaneous Metastasis of KHT Murine Tumors
Cancer Res., December 1, 2001; 61(24): 8903 - 8908.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
V. Vukovic, H. K. Haugland, T. Nicklee, A. J. Morrison, and D. W. Hedley
Hypoxia-inducible Factor-1{alpha} Is an Intrinsic Marker for Hypoxia in Cervical Cancer Xenografts
Cancer Res., October 1, 2001; 61(20): 7394 - 7398.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
F. U. Nielsen, P. Daugaard, L. Bentzen, H. Stodkilde-Jorgensen, J. Overgaard, M. R. Horsman, and R. J. Maxwell
Effect of Changing Tumor Oxygenation on Glycolytic Metabolism in a Murine C3H Mammary Carcinoma Assessed by in Vivo Nuclear Magnetic Resonance Spectroscopy
Cancer Res., July 1, 2001; 61(13): 5318 - 5325.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
R. D. Braun, J. L. Lanzen, S. A. Snyder, and M. W. Dewhirst
Comparison of tumor and normal tissue oxygen tension measurements using OxyLite or microelectrodes in rodents
Am J Physiol Heart Circ Physiol, June 1, 2001; 280(6): H2533 - H2544.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
D. M. Aebersold, P. Burri, K. T. Beer, J. Laissue, V. Djonov, R. H. Greiner, and G. L. Semenza
Expression of Hypoxia-inducible Factor-1{{alpha}}: A Novel Predictive and Prognostic Parameter in the Radiotherapy of Oropharyngeal Cancer
Cancer Res., April 1, 2001; 61(7): 2911 - 2916.
[Abstract] [Full Text]

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 Clin. Cancer Res.Home page
R. Airley, J. Loncaster, S. Davidson, M. Bromley, S. Roberts, A. Patterson, R. Hunter, I. Stratford, and C. West
Glucose Transporter Glut-1 Expression Correlates with Tumor Hypoxia and Predicts Metastasis-free Survival in Advanced Carcinoma of the Cervix
Clin. Cancer Res., April 1, 2001; 7(4): 928 - 934.
[Abstract] [Full Text]

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 JNCI J Natl Cancer InstHome page
M. Hockel and P. Vaupel
Tumor Hypoxia: Definitions and Current Clinical, Biologic, and Molecular Aspects
J Natl Cancer Inst, February 21, 2001; 93(4): 266 - 276.
[Abstract] [Full Text] [PDF]

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 JNCI J Natl Cancer InstHome page
R. Bos, H. Zhong, C. F. Hanrahan, E. C. M. Mommers, G. L. Semenza, H. M. Pinedo, M. D. Abeloff, J. W. Simons, P. J. van Diest, and E. van der Wall
Levels of Hypoxia-Inducible Factor-1{{alpha}} During Breast Carcinogenesis
J Natl Cancer Inst, February 21, 2001; 93(4): 309 - 314.
[Abstract] [Full Text] [PDF]

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 Cancer Res.Home page
N. C. Denko and A. J. Giaccia
Tumor Hypoxia, the Physiological Link between Trousseau's Syndrome (Carcinoma-induced Coagulopathy) and Metastasis
Cancer Res., February 1, 2001; 61(3): 795 - 798.
[Full Text]

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 JNMHome page
P. Burgman, J. A. O'Donoghue, J. L. Humm, and C. C. Ling
Hypoxia-Induced Increase in FDG Uptake in MCF7 Cells
J. Nucl. Med., January 1, 2001; 42(1): 170 - 175.
[Abstract] [Full Text] [PDF]


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