Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

Keynote webinar | Spotlight on sleep in brain health

LIVE: Thursday 2nd May 2024, 18:00-19:30 (CEST)

Quality sleep is essential for health. But what happens to our brains when sleep patterns are disturbed? Join our experts to explore the interplay between sleep disruption and neurological diseases, and the questions that you need to be asking your patients to help you prevent the harmful effects of sleep deprivation.
ADVANCED SEARCH
Log in
Top
BMC Cancer
Published in: BMC Cancer 1/2013

Open Access 01-12-2013 | Research article

Evaluation of hypoxia in a feline model of head and neck cancer using 64Cu-ATSM positron emission tomography/computed tomography

Authors: Elizabeth A Ballegeer, Nicole J Madrill, Kevin L Berger, Dalen W Agnew, Elizabeth A McNiel

Published in: BMC Cancer | Issue 1/2013

Login to get access

Abstract

Background

Human and feline head and neck squamous cell carcinoma (HNSCC) share histology, certain molecular features, as well as locally aggressive and highly recurrent clinical behavior. In human HNSCC, the presence of significant hypoxia within these tumors is considered an important factor in the development of a more aggressive phenotype and poor response to therapy. We hypothesized that feline head and neck tumors, particularly HNSCC, would exhibit hypoxia and that 64Cu-diacetyl-bis(N4-methylthiosemicarbazone) (Cu-ATSM) positron emission tomography/computed tomography (PET/CT) would permit detection of intratumoral hypoxia.

Methods

12 cats with measureable head and neck tumors were given 64Cu-ATSM and iodinated contrast for PET/CT scan. The presence or absence of hypoxia was also assessed using an intratumoral fluorescent life-time probe to quantitate pO2 and pimonidazole immunohistochemical staining in biopsy specimens. In two cats, intratumoral O2 and 64Cu-ATSM uptake was measured before and after treatment with anti-angiogenic agents to determine the effect of these agents on hypoxia.

Results

Eleven of twelve feline tumors demonstrated significant 64Cu-ATSM uptake, regardless of malignant or benign etiology. The presence (and absence) of hypoxia was confirmed using the fluorescent O2 detection probe in nine tumors, and using pimonidazole staining in three tumors. Squamous cell carcinomas (HNSCC) demonstrated the highest degree of hypoxia, with Tmax/M ratios ranging from 4.3 to 21.8. Additional non-neoplastic tissues exhibited 64Cu-ATSM uptake suggestive of hypoxia including reactive draining lymph nodes, non-malignant thyroid pathology, a tooth root abscess, and otitis media. In two cats with HNSCC that received anti-vascular agents, the pattern of 64Cu-ATSM uptake was altered after treatment, demonstrating the potential of the feline model to study the modulation of tumor oxygenation.

Conclusion

Feline HNSCC serves as a clinically relevant model for the investigation of intratumoral hypoxia including its measurement, modulation and targeting.
Appendix
Available only for authorised users
Literature
1.
Jain RK: Normalization of tumor vasculature: an emerging concept in antiangiogenic therapy. Science. 2005, 307 (5706): 58-62. 10.1126/science.1104819.CrossRefPubMed
2.
Vaupel P: Tumor microenvironmental physiology and its implications for radiation oncology. Semin Radiat Oncol. 2004, 14 (3): 198-206. 10.1016/j.semradonc.2004.04.008.CrossRefPubMed
3.
Padera TP, Stoll BR, Tooredman JB, Capen D, di Tomaso E, Jain RK: Pathology: cancer cells compress intratumour vessels. Nature. 2004, 427 (6976): 695-10.1038/427695a.CrossRefPubMed
4.
Vaupel P, Mayer A: Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev. 2007, 26 (2): 225-239. 10.1007/s10555-007-9055-1.CrossRefPubMed
5.
Hall EJ, Giaccia AJ: Oxygen effec and re-oxygenation. Radiobiology for the Radiologist. Edited by: Hall EJ, Giaccia AJ. 2012, Philadelphia: Lipponcott, Williams & Wilkins, 7
6.
Eckert AW, Lautner MH, Schutze A, Taubert H, Schubert J, Bilkenroth U: Coexpression of hypoxia-inducible factor-1alpha and glucose transporter-1 is associated with poor prognosis in oral squamous cell carcinoma patients. Histopathology. 2011, 58 (7): 1136-1147. 10.1111/j.1365-2559.2011.03806.x.CrossRefPubMed
7.
Hockel M, Knoop C, Schlenger K, Vorndran B, Baussmann E, Mitze M, Knapstein PG, Vaupel P: Intratumoral pO2 predicts survival in advanced cancer of the uterine cervix. Radiother Oncol. 1993, 26 (1): 45-50. 10.1016/0167-8140(93)90025-4.CrossRefPubMed
8.
Perez-Sayans M, Somoza-Martin JM, Barros-Angueira F, Diz PG, Rey JM, Garcia-Garcia A: Multidrug resistance in oral squamous cell carcinoma: the role of vacuolar ATPases. Cancer Lett. 2010, 295 (2): 135-143. 10.1016/j.canlet.2010.03.019.CrossRefPubMed
9.
Perez-Sayans M, Suarez-Penaranda JM, Pilar GD, Barros-Angueira F, Gandara-Rey JM, Garcia-Garcia A: Hypoxia-inducible factors in OSCC. Cancer Lett. 2011, 313 (1): 1-8. 10.1016/j.canlet.2011.08.017.CrossRefPubMed
10.
Unruh A, Ressel A, Mohamed HG, Johnson RS, Nadrowitz R, Richter E, Katschinski DM, Wenger RH: The hypoxia-inducible factor-1 alpha is a negative factor for tumor therapy. Oncogene. 2003, 22 (21): 3213-3220. 10.1038/sj.onc.1206385.CrossRefPubMed
11.
Roh JL, Cho KJ, Kwon GY, Ryu CH, Chang HW, Choi SH, Nam SY, Kim SY: The prognostic value of hypoxia markers in T2-staged oral tongue cancer. Oral Oncol. 2009, 45 (1): 63-68. 10.1016/j.oraloncology.2008.03.017.CrossRefPubMed
12.
Brizel DM, Sibley GS, Prosnitz LR, Scher RL, Dewhirst MW: Tumor hypoxia adversely affects the prognosis of carcinoma of the head and neck. Int J Radiat Oncol Biol Phys. 1997, 38 (2): 285-289. 10.1016/S0360-3016(97)00101-6.CrossRefPubMed
13.
Bowen SR, van der Kogel AJ, Nordsmark M, Bentzen SM, Jeraj R: Characterization of positron emission tomography hypoxia tracer uptake and tissue oxygenation via electrochemical modeling. Nucl Med Biol. 2011, 38 (6): 771-780. 10.1016/j.nucmedbio.2011.02.002.CrossRefPubMedPubMedCentral
14.
Kikuchi M, Yamane T, Shinohara S, Fujiwara K, Hori SY, Tona Y, Yamazaki H, Naito Y, Senda M: 18F-fluoromisonidazole positron emission tomography before treatment is a predictor of radiotherapy outcome and survival prognosis in patients with head and neck squamous cell carcinoma. Ann Nucl Med. 2011, 25 (9): 625-633. 10.1007/s12149-011-0508-9.CrossRefPubMed
15.
Maftei CA, Shi K, Bayer C, Astner ST, Vaupel P: Comparison of (immuno-)fluorescence data with serial [(1)(8)F]Fmiso PET/CT imaging for assessment of chronic and acute hypoxia in head and neck cancers. Radiother Oncol. 2011, 99 (3): 412-417. 10.1016/j.radonc.2011.05.079.CrossRefPubMed
16.
O'Donoghue JA, Zanzonico P, Pugachev A, Wen B, Smith-Jones P, Cai S, Burnazi E, Finn RD, Burgman P, Ruan S: Assessment of regional tumor hypoxia using 18F-fluoromisonidazole and 64Cu(II)-diacetyl-bis(N4-methylthiosemicarbazone) positron emission tomography: comparative study featuring microPET imaging, pOo2 probe measurement, autoradiography, and fluorescent microscopy in the R3327-AT and FaDu rat tumor models. Int J Radiat Oncol Biol Phys. 2005, 61 (5): 1493-1502. 10.1016/j.ijrobp.2004.12.057.CrossRefPubMed
17.
Yamada T, Uchida M, Kwang-Lee K, Kitamura N, Yoshimura T, Sasabe E, Yamamoto T: Correlation of metabolism/hypoxia markers and fluorodeoxyglucose uptake in oral squamous cell carcinomas. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2012, 113 (4): 464-471. 10.1016/j.tripleo.2011.04.006.CrossRef
18.
Overgaard J: Hypoxic modification of radiotherapy in squamous cell carcinoma of the head and neck—a systematic review and meta-analysis. Radiother Oncol. 2011, 100 (1): 22-32. 10.1016/j.radonc.2011.03.004.CrossRefPubMed
19.
Liptak JM, Withrow SJ: Oral tumors. Withrow and MacEwen's Small Animal Clinical Oncology. Volume 4th. Edited by: Withrow SJ, Vail DM. 2007, St. Louis: Saunders Elsevier Inc, 455-510.
20.
Dorn CR, Priester WA: Epidemiologic analysis of oral and pharyngeal cancer in dogs, cats, horses, and cattle. J Am Vet Med Assoc. 1976, 169 (11): 1202-1206.PubMed
21.
Bertone ER, Snyder LA, Moore AS: Environmental and lifestyle risk factors for oral squamous cell carcinoma in domestic cats. J Vet Intern Med. 2003, 17 (4): 557-562. 10.1111/j.1939-1676.2003.tb02478.x.CrossRefPubMed
22.
McNiel EA, Carmella SG, Heath LA, Bliss RL, Le KA, Hecht SS: Urinary biomarkers to assess exposure of cats to environmental tobacco smoke. Am J Vet Res. 2007, 68 (4): 349-353. 10.2460/ajvr.68.4.349.CrossRefPubMed
23.
Snyder LA, Bertone ER, Jakowski RM, Dooner MS, Jennings-Ritchie J, Moore AS: p53 expression and environmental tobacco smoke exposure in feline oral squamous cell carcinoma. Vet Pathol. 2004, 41 (3): 209-214. 10.1354/vp.41-3-209.CrossRefPubMed
24.
Looper JS, Malarkey DE, Ruslander D, Proulx D, Thrall DE: Epidermal growth factor receptor expression in feline oral squamous cell carcinomas. Vet Comp Oncol. 2006, 4 (1): 33-40. 10.1111/j.1476-5810.2006.00091.x.CrossRefPubMed
25.
Sabattini S, Marconato L, Zoff A, Morini M, Scarpa F, Capitani O, Bettini G: Epidermal growth factor receptor expression is predictive of poor prognosis in feline cutaneous squamous cell carcinoma. J Feline Med Surg. 2010, 12 (10): 760-768. 10.1016/j.jfms.2010.04.010.CrossRefPubMed
26.
Beam SL, Rassnick KM, Moore AS, McDonough SP: An immunohistochemical study of cyclooxygenase-2 expression in various feline neoplasms. Vet Pathol. 2003, 40 (5): 496-500. 10.1354/vp.40-5-496.CrossRefPubMed
27.
Hayes A, Scase T, Miller J, Murphy S, Sparkes A, Adams V: COX-1 and COX-2 expression in feline oral squamous cell carcinoma. J Comp Pathol. 2006, 135 (2–3): 93-99.CrossRefPubMed
28.
DiBernardi L, Dore M, Davis JA, Owens JG, Mohammed SI, Guptill CF, Knapp DW: Study of feline oral squamous cell carcinoma: potential target for cyclooxygenase inhibitor treatment. Prostaglandins Leukot Essent Fat Acids. 2007, 76 (4): 245-250. 10.1016/j.plefa.2007.01.006.CrossRef
29.
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 (5): 237-255. 10.1002/1097-0215(20001020)90:5<237::AID-IJC1>3.0.CO;2-T.CrossRefPubMed
30.
Bruehlmeier M, Kaser-Hotz B, Achermann R, Bley CR, Wergin M, Schubiger PA, Ametamey SM: Measurement of tumor hypoxia in spontaneous canine sarcomas. Vet Radiol Ultrasound. 2005, 46 (4): 348-354. 10.1111/j.1740-8261.2005.00065.x.CrossRefPubMed
31.
Foo SS, Abbott DF, Lawrentschuk N, Scott AM: Functional imaging of intratumoral hypoxia. Mol Imaging Biol. 2004, 6 (5): 291-305. 10.1016/j.mibio.2004.06.007.CrossRefPubMed
32.
Yuan H, Schroeder T, Bowsher JE, Hedlund LW, Wong T, Dewhirst MW: Intertumoral differences in hypoxia selectivity of the PET imaging agent 64Cu(II)-diacetyl-bis(N4-methylthiosemicarbazone). J Nucl Med. 2006, 47 (6): 989-998.PubMed
33.
Azuma C, Raleigh JA, Thrall DE: Longevity of pimonidazole adducts in spontaneous canine tumors as an estimate of hypoxic cell lifetime. Radiat Res. 1997, 148 (1): 35-42. 10.2307/3579536.CrossRefPubMed
34.
Kleiter MM, Thrall DE, Malarkey DE, Ji X, Lee DY, Chou SC, Raleigh JA: A comparison of oral and intravenous pimonidazole in canine tumors using intravenous CCI-103F as a control hypoxia marker. Int J Radiat Oncol Biol Phys. 2006, 64 (2): 592-602. 10.1016/j.ijrobp.2005.09.010.CrossRefPubMed
35.
Raleigh JA, Chou SC, Bono EL, Thrall DE, Varia MA: Semiquantitative immunohistochemical analysis for hypoxia in human tumors. Int J Radiat Oncol Biol Phys. 2001, 49 (2): 569-574. 10.1016/S0360-3016(00)01505-4.CrossRefPubMed
36.
Griffioen AW, van der Schaft DW, Barendsz-Janson AF, Cox A, Struijker Boudier HA, Hillen HF, Mayo KH: Anginex, a designed peptide that inhibits angiogenesis. Biochem J. 2001, 354 (Pt 2): 233-242.CrossRefPubMedPubMedCentral
37.
Kubota K, Matsuzawa T, Ito M, Ito K, Fujiwara T, Abe Y, Yoshioka S, Fukuda H, Hatazawa J, Iwata R: Lung tumor imaging by positron emission tomography using C-11 L-methionine. J Nucl Med. 1985, 26 (1): 37-42.PubMed
38.
Eisenhauer EA, Therasse P, Bogaerts J, Schwartz LH, Sargent D, Ford R, Dancey J, Arbuck S, Gwyther S, Mooney M: New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). Eur J Cancer. 2009, 45 (2): 228-247. 10.1016/j.ejca.2008.10.026.CrossRefPubMed
39.
Hall EJ, Giaccia AJ: Oxygen effect and reoxygenation. Radiobiology for the Radiologist. Volume 7th. Edited by: Hall EJ, Giacca AJ. 2012, Philadephia: Lippincott, Williams & Wilkins, 86-103.
40.
Kawakami K, Hattori M, Inoue T, Maruyama Y, Ohkanda J, Kato N, Tongu M, Yamada T, Akimoto M, Takenaga K: A novel fusicoccin derivative preferentially targets hypoxic tumor cells and inhibits growth in xenografts. Anti Cancer Agents Med Chem. 2012, 17 (7): 791-800.CrossRef
41.
Citrin D, Camphausen K: Advancement of antiangiogenic and vascular disrupting agents combined with radiation. Radiation Oncology Advances. Edited by: Bentzen SM, Harari PM, Tome WA, Mehta MP. 2008, New York: Springer, LLC, 153-172.
42.
Tatum JL, Kelloff GJ, Gillies RJ, Arbeit JM, Brown JM, Chao KS, Chapman JD, Eckelman WC, Fyles AW, Giaccia AJ: Hypoxia: importance in tumor biology, noninvasive measurement by imaging, and value of its measurement in the management of cancer therapy. Int J Radiat Biol. 2006, 82 (10): 699-757. 10.1080/09553000601002324.CrossRefPubMed
43.
Smith LP, Thomas GR: Animal models for the study of squamous cell carcinoma of the upper aerodigestive tract: a historical perspective with review of their utility and limitations. Part A. Chemically-induced de novo cancer, syngeneic animal models of HNSCC, animal models of transplanted xenogeneic human tumors. Int J Cancer. 2006, 118 (9): 2111-2122. 10.1002/ijc.21694.CrossRefPubMed
44.
Padhani AR, Krohn KA, Lewis JS, Alber M: Imaging oxygenation of human tumours. Eur Radiol. 2007, 17 (4): 861-872. 10.1007/s00330-006-0431-y.CrossRefPubMed
45.
Wood KA, Wong WL, Saunders MI: [(64)Cu]diacetyl-bis(N(4)-methyl-thiosemicarbazone)—a radiotracer for tumor hypoxia. Nucl Med Biol. 2008, 35 (4): 393-400. 10.1016/j.nucmedbio.2008.02.002.CrossRefPubMed
46.
Yoshii Y, Furukawa T, Kiyono Y, Watanabe R, Mori T, Yoshii H, Asai T, Okazawa H, Welch MJ, Fujibayashi Y: Internal radiotherapy with copper-64-diacetyl-bis (N4-methylthiosemicarbazone) reduces CD133+ highly tumorigenic cells and metastatic ability of mouse colon carcinoma. Nucl Med Biol. 2011, 38 (2): 151-157. 10.1016/j.nucmedbio.2010.08.009.CrossRefPubMed
47.
Weeks AJ, Paul RL, Marsden PK, Blower PJ, Lloyd DR: Radiobiological effects of hypoxia-dependent uptake of 64Cu-ATSM: enhanced DNA damage and cytotoxicity in hypoxic cells. Eur J Nucl Med Mol Imaging. 2010, 37 (2): 330-338. 10.1007/s00259-009-1305-8.CrossRefPubMed
48.
Vavere AL, Lewis JS: Cu-ATSM: a radiopharmaceutical for the PET imaging of hypoxia. Dalton Trans. 2007, 43: 4893-4902.CrossRefPubMed
49.
de Lussanet QG, Beets-Tan RG, Backes WH, van der Schaft DW, van Engelshoven JM, Mayo KH, Griffioen AW, Beets-Tan RGH, van der Schaft DWJ, van Engelshoven JMA: Dynamic contrast-enhanced magnetic resonance imaging at 1.5 Tesla with gadopentetate dimeglumine to assess the angiostatic effects of anginex in mice. Eur J Cancer. 2004, 40 (8): 1262-1268. 10.1016/j.ejca.2004.01.020.CrossRefPubMed
50.
Black NF, McJames S, Rust TC, Kadrmas DJ: Evaluation of rapid dual-tracer (62)Cu-PTSM + (62)Cu-ATSM PET in dogs with spontaneously occurring tumors. Phys Med Biol. 2008, 53 (1): 217-232. 10.1088/0031-9155/53/1/015.CrossRefPubMed
51.
Dietz DW, Dehdashti F, Grigsby PW, Malyapa RS, Myerson RJ, Picus J, Ritter J, Lewis JS, Welch MJ, Siegel BA: Tumor hypoxia detected by positron emission tomography with 60Cu-ATSM as a predictor of response and survival in patients undergoing Neoadjuvant chemoradiotherapy for rectal carcinoma: a pilot study. Dis Colon Rectum. 2008, 51 (11): 1641-1648. 10.1007/s10350-008-9420-3.CrossRefPubMed
52.
Lewis JS, Sharp TL, Laforest R, Fujibayashi Y, Welch MJ: Tumor uptake of copper-diacetyl-bis(N(4)-methylthiosemicarbazone): effect of changes in tissue oxygenation. J Nucl Med. 2001, 42 (4): 655-661.PubMed
53.
Minagawa Y, Shizukuishi K, Koike I, Horiuchi C, Watanuki K, Hata M, Omura M, Odagiri K, Tohnai I, Inoue T: Assessment of tumor hypoxia by 62Cu-ATSM PET/CT as a predictor of response in head and neck cancer: a pilot study. Ann Nucl Med. 2011, 25 (5): 339-345. 10.1007/s12149-011-0471-5.CrossRefPubMed
54.
Ikawa M, Okazawa H, Kudo T, Kuriyama M, Fujibayashi Y, Yoneda M: Evaluation of striatal oxidative stress in patients with Parkinson's disease using [62Cu]ATSM PET. Nucl Med Biol. 2011, 38 (7): 945-951. 10.1016/j.nucmedbio.2011.02.016.CrossRefPubMed
55.
Skovgaard D, Kjaer M, Madsen J, Kjaer A: Noninvasive 64Cu-ATSM and PET/CT assessment of hypoxia in rat skeletal muscles and tendons during muscle contractions. J Nucl Med. 2009, 50 (6): 950-958. 10.2967/jnumed.109.062216.CrossRefPubMed
56.
Dehdashti F, Grigsby PW, Mintun MA, Lewis JS, Siegel BA, Welch MJ: Assessing tumor hypoxia in cervical cancer by positron emission tomography with 60Cu-ATSM: relationship to therapeutic response-a preliminary report.Int J Radiat Oncol Biol Phys. 2003, 55 (5): 1233-1238. 10.1016/S0360-3016(02)04477-2.CrossRefPubMed
57.
Nathan SS, DiResta GR, Casas-Ganem JE, Hoang BH, Sowers R, Yang R, Huvos AG, Gorlick R, Healey JH: Elevated physiologic tumor pressure promotes proliferation and chemosensitivity in human osteosarcoma. Clin Cancer Res. 2005, 11 (6): 2389-2397. 10.1158/1078-0432.CCR-04-2048.CrossRefPubMed
58.
Nathan SS, Huvos AG, Casas-Ganem JE, Yang R, Linkov I, Sowers R, DiResta GR, Gorlick R, Healey JH: Tumour interstitial fluid pressure may regulate angiogenic factors in osteosarcoma. Ann Acad Med Singap. 2009, 38 (12): 1041-1047.PubMed
59.
Zachos TA, Aiken SW, DiResta GR, Healey JH: Interstitial fluid pressure and blood flow in canine osteosarcoma and other tumors. Clin Orthop Relat Res. 2001, 385: 230-236.CrossRefPubMed
60.
Dehdashti F, Mintun MA, Lewis JS, Bradley J, Govindan R, Laforest R, Welch MJ, Siegel BA: In vivo assessment of tumor hypoxia in lung cancer with 60Cu-ATSM. Eur J Nucl Med Mol Imaging. 2003, 30 (6): 844-850. 10.1007/s00259-003-1130-4.CrossRefPubMed
61.
Gagel B, Reinartz P, Dimartino E, Zimny M, Pinkawa M, Maneschi P, Stanzel S, Hamacher K, Coenen HH, Westhofen M: pO(2) polarography versus positron emission tomography ([(18)F] fluoromisonidazole, [(18)F]-2-fluoro-2'-deoxyglucose). An appraisal of radiotherapeutically relevant hypoxia. Strahlenther Onkol. 2004, 180 (10): 616-622. 10.1007/s00066-004-1229-y.CrossRefPubMed
62.
Postema EJ, McEwan AJ, Riauka TA, Kumar P, Richmond DA, Abrams DN, Wiebe LI: Initial results of hypoxia imaging using 1-alpha-D: -(5-deoxy-5-[18F]-fluoroarabinofuranosyl)-2-nitroimidazole (18F-FAZA). Eur J Nucl Med Mol Imaging. 2009, 36 (10): 1565-1573. 10.1007/s00259-009-1154-5.CrossRefPubMed
63.
Cheeseman MT, Tyrer HE, Williams D, Hough TA, Pathak P, Romero MR, Hilton H, Bali S, Parker A, Vizor L: HIF-VEGF pathways are critical for chronic otitis media in Junbo and Jeff mouse mutants. PLoS Genet. 2011, 7 (10): e1002336-10.1371/journal.pgen.1002336.CrossRefPubMedPubMedCentral
64.
Peterson ME: Hyperthyroidism. Textbook of Veterinary Internal Medicine. Edited by: Ettinger SJ, Feldman EC. 2000, Philadelphia: W.B. Saunders, 1400-1419.
65.
Itoh A, Iwase K, Jimbo S, Yamamoto H, Yamamoto N, Kokubo M, Senda T, Nakai A, Nagagasaka A, Nagasaka T: Expression of vascular endothelial growth factor and presence of angiovascular cells in tissues from different thyroid disorders. World J Surg. 2010, 34 (2): 242-248. 10.1007/s00268-009-0344-4.CrossRefPubMed
66.
Zhong Z, Li X, Yamashina S, von Frankenberg M, Enomoto N, Ikejima K, Kolinsky M, Raleigh JA, Thurman RG: Cyclosporin A causes a hypermetabolic state and hypoxia in the liver: prevention by dietary glycine. J Pharmacol Exp Ther. 2001, 299 (3): 858-865.PubMed
67.
Cook GJ, Houston S, Barrington SF, Fogelman I: Technetium-99m-labeled HL91 to identify tumor hypoxia: correlation with fluorine-18-FDG. J Nucl Med. 1998, 39 (1): 99-103.PubMed
68.
Dings RP, Loren M, Heun H, McNiel E, Griffioen AW, Mayo KH, Griffin RJ, Dings RPM, Loren M, Heun H: Scheduling of radiation with angiogenesis inhibitors anginex and Avastin improves therapeutic outcome via vessel normalization. Clin Cancer Res. 2007, 13 (11): 3395-3402. 10.1158/1078-0432.CCR-06-2441.CrossRefPubMedPubMedCentral
Metadata
Title
Evaluation of hypoxia in a feline model of head and neck cancer using 64Cu-ATSM positron emission tomography/computed tomography
Authors
Elizabeth A Ballegeer
Nicole J Madrill
Kevin L Berger
Dalen W Agnew
Elizabeth A McNiel
Publication date
01-12-2013
Publisher
BioMed Central
Published in
BMC Cancer / Issue 1/2013
Electronic ISSN: 1471-2407
DOI
https://doi.org/10.1186/1471-2407-13-218

Other articles of this Issue 1/2013

BMC Cancer 1/2013 Go to the issue

Research article

Primary Tumor Vascularity, HIF-1α and VEGF expression in vulvar squamous cell carcinomas: their relationships with clinicopathological characteristics and prognostic impact

Editorial

Recognizing the role of surgical oncology and cancer imaging in the multidisciplinary approach to cancer: an important area of future scholarly growth for BMC Cancer

Research article

Clinical complete responders to definite chemoradiation or radiation therapy for oesophageal cancer: predictors of outcome

Research article

Radiation mitigating properties of the lignan component in flaxseed

Study protocol

A prospective investigation of predictive and modifiable risk factors for breast cancer in unaffected BRCA1 and BRCA2gene carriers

Research article

Multicenter phase II study of weekly docetaxel, cisplatin, and S-1 (TPS) induction chemotherapy for locally advanced squamous cell cancer of the head and neck
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine
Image Credits