Skip to main content
SpringerLink
Log in

Review of Tissue Oxygenation Sensing During Radiotherapy Based Upon Cherenkov-Excited Luminescence Imaging

  • Review
  • Published:
Applied Magnetic Resonance Aims and scope Submit manuscript

Abstract

Oxygen sensing with light has been developing for many decades using injectable molecules called Oxyphors, which are pegylated, dendrimer-encapsulated metalloporphyrins that have a phosphorescence emission lifetime that is a direct reporter of the local oxygen partial pressure (pO2). In recent years, the ability to image this emission from tissue with Cherenkov light excitation during high-energy X-ray-based radiation therapy has been shown and developed for research studies. The main value of this type of lifetime-based pO2 sensing, termed Cherenkov-Excited Luminescence Imaging (CELI) is in its ability to image values of pO2 from within the tissue during radiation therapy using tracers that are systemic and biologically compatible. Spatial mapping of pO2 can realized either as surface imaging or deep tissue tomography through a few centimeters. The

spatial resolution is radiation dose-dependent but can be near 0.1 mm, based upon radiation doses expected in a fractionated treatment plan. When imaging tumors with a broad beam irradiation, histograms of pO2 values across the surface have been demonstrated illustrating microscopic sensitivity to the ranges of oxygen levels present, and the ability to track these microscopic histograms during daily fractionated radiation therapy is possible. The pO2 distributions provide for sensitivity to the hypoxic fraction of the tumor—a unique capability of oxygen imaging that has microscopic spatial sampling. Comparisons of the CELI pO2 method to other oxygen-sensing methods, as well as the ability to use the CELI technique as a tool to examine the optimization of radiation therapy treatment technique is ongoing.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Availability of data and material

n/a.

Code availability

n/a.

References

  1. H.M. Swartz, P. Vaupel, B.B. Williams, P.E. Schaner, B. Gallez, W. Schreiber, A. Ali, A.B. Flood, ’Oxygen level in a tissue’—what do available measurements really report? Adv Exp Med Biol 1232, 145–153 (2020)

    Article  Google Scholar 

  2. H.M. Swartz, A.B. Flood, P.E. Schaner, H. Halpern, B.B. Williams, B.W. Pogue, B. Gallez, P. Vaupel, How best to interpret measures of levels of oxygen in tissues to make them effective clinical tools for care of patients with cancer and other oxygen-dependent pathologies. Physiol Rep 8(15), e14541 (2020)

    Article  Google Scholar 

  3. X. Cao, S.R. Allu, S. Jiang, J.R. Gunn, C. Yao, J. Xin, P. Bruza, D.J. Gladstone, L.A. Jarvis, J. Tian, H.M. Swartz, S.A. Vinogradov, B.W. Pogue, High resolution pO2 imaging improves quantification of the hypoxic fraction in tumors during radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 109, 603–613 (2020)

    Article  Google Scholar 

  4. X. Cao, R. Zhang, T.V. Esipova, S.R. Allu, R. Ashraf, M. Rahman, J.R. Gunn, P. Bruza, D.J. Gladstone, B.B. Williams, H.M. Swartz, P.J. Hoopes, S.A. Vinogradov, B.W. Pogue, Quantification of oxygen depletion during FLASH irradiation in vitro and in vivo. Int. J. Radiat. Oncol. Biol. Phys. 111(1), 240–248 (2021)

  5. P. Vaupel, O. Thews, D.K. Kelleher, M. Hoeckel, Oxygenation of human tumors: the Mainz experience. Strahlenther Onkol 174(Suppl 4), 6–12 (1998)

    Google Scholar 

  6. M. Hockel, K. Schlenger, S. Hockel, B. Aral, U. Schaffer, P. Vaupel, Tumor hypoxia in pelvic recurrences of cervical cancer. Int. J. Cancer 79(4), 365–369 (1998)

    Article  Google Scholar 

  7. H.M. Swartz, B.B. Williams, B.I. Zaki, A.C. Hartford, L.A. Jarvis, E.Y. Chen, R.J. Comi, M.S. Ernstoff, H. Hou, N. Khan, S.G. Swarts, A.B. Flood, P. Kuppusamy, Clinical EPR: unique opportunities and some challenges. Acad. Radiol. 21(2), 197–206 (2014)

    Article  Google Scholar 

  8. H.M. Swartz, H. Hou, N. Khan, L.A. Jarvis, E.Y. Chen, B.B. Williams, P. Kuppusamy, Advances in probes and methods for clinical EPR oximetry. Adv. Exp. Med. Biol. 812, 73–79 (2014)

    Article  Google Scholar 

  9. S. Lock, R. Perrin, A. Seidlitz, A. Bandurska-Luque, S. Zschaeck, K. Zophel, M. Krause, J. Steinbach, J. Kotzerke, D. Zips, E.G.C. Troost, M. Baumann, Residual tumour hypoxia in head-and-neck cancer patients undergoing primary radiochemotherapy, final results of a prospective trial on repeat FMISO-PET imaging. Radiother. Oncol. 124(3), 533–540 (2017)

    Article  Google Scholar 

  10. S. Lock, A. Linge, A. Seidlitz, A. Bandurska-Luque, A. Nowak, V. Gudziol, F. Buchholz, D.E. Aust, G.B. Baretton, K. Zophel, J. Steinbach, J. Kotzerke, J. Overgaard, D. Zips, M. Krause, M. Baumann, E.G.C. Troost, Repeat FMISO-PET imaging weakly correlates with hypoxia-associated gene expressions for locally advanced HNSCC treated by primary radiochemotherapy. Radiother. Oncol. 135, 43–50 (2019)

    Article  Google Scholar 

  11. S. Zhao, W. Yu, N. Ukon, C. Tan, K.I. Nishijima, Y. Shimizu, K. Higashikawa, T. Shiga, H. Yamashita, N. Tamaki, Y. Kuge, Elimination of tumor hypoxia by eribulin demonstrated by (18)F-FMISO hypoxia imaging in human tumor xenograft models. EJNMMI Res. 9(1), 51 (2019)

    Article  Google Scholar 

  12. E.R. Gerstner, Z. Zhang, J.R. Fink, M. Muzi, L. Hanna, E. Greco, M. Prah, K.M. Schmainda, A. Mintz, L. Kostakoglu, E.A. Eikman, B.M. Ellingson, E.M. Ratai, A.G. Sorensen, D.P. Barboriak, D.A. Mankoff, A.T. Group, ACRIN 6684: assessment of tumor hypoxia in newly diagnosed glioblastoma using 18F-FMISO PET and MRI. Clin. Cancer Res. 22(20), 5079–5086 (2016)

    Article  Google Scholar 

  13. S. Zschaeck, K. Zophel, A. Seidlitz, D. Zips, J. Kotzerke, M. Baumann, E.G.C. Troost, S. Lock, M. Krause, Generation of biological hypotheses by functional imaging links tumor hypoxia to radiation induced tissue inflammation/glucose uptake in head and neck cancer. Radiother Oncol 155, 204–211 (2021)

    Article  Google Scholar 

  14. L. Wang, H. Wang, K. Shen, H. Park, T. Zhang, X. Wu, M. Hu, H. Yuan, Y. Chen, Z. Wu, Q. Wang, Z. Li, Development of novel (18)F-PET agents for tumor hypoxia imaging. J. Med. Chem. 64(9), 5593–5602 (2021)

    Article  Google Scholar 

  15. P. Vera, S.D. Mihailescu, J. Lequesne, R. Modzelewski, P. Bohn, S. Hapdey, L.F. Pepin, B. Dubray, P. Chaumet-Riffaud, P. Decazes, S. Thureau, R.S. all investigators of, Radiotherapy boost in patients with hypoxic lesions identified by (18)F-FMISO PET/CT in non-small-cell lung carcinoma: can we expect a better survival outcome without toxicity? [RTEP5 long-term follow-up]. Eur. J. Nucl. Med. Mol. Imaging 46(7), 1448–1456 (2019)

    Article  Google Scholar 

  16. S.G. Peeters, C.M. Zegers, N.G. Lieuwes, W. van Elmpt, J. Eriksson, G.A. van Dongen, L. Dubois, P. Lambin, A comparative study of the hypoxia PET tracers [(1)(8)F]HX4, [(1)(8)F]FAZA, and [(1)(8)F]FMISO in a preclinical tumor model. Int. J. Radiat. Oncol. Biol. Phys. 91(2), 351–359 (2015)

    Article  Google Scholar 

  17. M. Busk, O.L. Munk, S. Jakobsen, T. Wang, M. Skals, T. Steiniche, M.R. Horsman, J. Overgaard, Assessing hypoxia in animal tumor models based on pharmocokinetic analysis of dynamic FAZA PET. Acta. Oncol. 49(7), 922–933 (2010)

    Article  Google Scholar 

  18. A. Mayer, A. Wree, M. Hockel, C. Leo, H. Pilch, P. Vaupel, Lack of correlation between expression of HIF-1alpha protein and oxygenation status in identical tissue areas of squamous cell carcinomas of the uterine cervix. Cancer Res. 64(16), 5876–5881 (2004)

    Article  Google Scholar 

  19. L.S. Mortensen, S. Buus, M. Nordsmark, L. Bentzen, O.L. Munk, S. Keiding, J. Overgaard, Identifying hypoxia in human tumors: a correlation study between 18F-FMISO PET and the Eppendorf oxygen-sensitive electrode. Acta. Oncol. 49(7), 934–940 (2010)

    Article  Google Scholar 

  20. C. Bayer, P. Vaupel, Acute versus chronic hypoxia in tumors: controversial data concerning time frames and biological consequences. Strahlenther. Onkol. 188(7), 616–627 (2012)

    Article  Google Scholar 

  21. I.J. Hoogsteen, H.A. Marres, A.J. van der Kogel, J.H. Kaanders, The hypoxic tumour microenvironment, patient selection and hypoxia-modifying treatments. Clin. Oncol. (R Coll. Radiol) 19(6), 385–396 (2007)

    Article  Google Scholar 

  22. B. Bachtiary, M. Schindl, R. Potter, B. Dreier, T.H. Knocke, J.A. Hainfellner, R. Horvat, P. Birner, Overexpression of hypoxia-inducible factor 1alpha indicates diminished response to radiotherapy and unfavorable prognosis in patients receiving radical radiotherapy for cervical cancer. Clin. Cancer Res. 9(6), 2234–2240 (2003)

    Google Scholar 

  23. L.B. Harrison, M. Chadha, R.J. Hill, K. Hu, D. Shasha, Impact of tumor hypoxia and anemia on radiation therapy outcomes. Oncologist 7(6), 492–508 (2002)

    Article  Google Scholar 

  24. R.M. Sutherland, Tumor hypoxia and gene expression–implications for malignant progression and therapy. Acta. Oncol. 37(6), 567–574 (1998)

    Article  Google Scholar 

  25. M. Hockel, K. Schlenger, M. Mitze, U. Schaffer, P. Vaupel, Hypoxia and radiation response in human tumors. Semin Radiat. Oncol. 6(1), 3–9 (1996)

    Article  Google Scholar 

  26. P. Vaupel, L. Harrison, Tumor hypoxia: causative factors, compensatory mechanisms, and cellular response. Oncologist 9(Suppl 5), 4–9 (2004)

    Article  Google Scholar 

  27. M. Nordsmark, S.M. Bentzen, V. Rudat, D. Brizel, E. Lartigau, P. Stadler, A. Becker, M. Adam, M. Molls, J. Dunst, D.J. Terris, J. Overgaard, Prognostic value of tumor oxygenation in 397 head and neck tumors after primary radiation therapy. An international multi-center study. Radiother. Oncol. 77(1), 18–24 (2005)

    Article  Google Scholar 

  28. M. Nordsmark, J. Loncaster, C. Aquino-Parsons, S.C. Chou, V. Gebski, C. West, J.C. Lindegaard, H. Havsteen, S.E. Davidson, R. Hunter, J.A. Raleigh, J. Overgaard, The prognostic value of pimonidazole and tumour pO2 in human cervix carcinomas after radiation therapy: a prospective international multi-center study. Radiother. Oncol. 80(2), 123–131 (2006)

    Article  Google Scholar 

  29. P. Vaupel, M. Hockel, A. Mayer, Detection and characterization of tumor hypoxia using pO2 histography. Antioxid. Redox Signal 9(8), 1221–1235 (2007)

    Article  Google Scholar 

  30. P. Vaupel, A. Mayer, M. Hockel, Oxygenation status of primary and recurrent squamous cell carcinomas of the vulva. Eur. J. Gynaecol. Oncol. 27(2), 142–146 (2006)

    Google Scholar 

  31. C. Menon, D.L. Fraker, Tumor oxygenation status as a prognostic marker. Cancer Lett. 221(2), 225–235 (2005)

    Article  Google Scholar 

  32. T.V. Esipova, M.J.P. Barrett, E. Erlebach, A.E. Masunov, B. Weber, S.A. Vinogradov, Oxyphor 2P: a high-performance probe for deep-tissue longitudinal oxygen imaging. Cell Metab. 29(3), 736 e7-744 e7 (2019)

    Article  Google Scholar 

  33. T.V. Esipova, A. Karagodov, J. Miller, D.F. Wilson, T.M. Busch, S.A. Vinogradov, Two new “protected” oxyphors for biological oximetry: properties and application in tumor imaging. Anal. Chem. 83(22), 8756–8765 (2011)

    Article  Google Scholar 

  34. L.S. Ziemer, W.M. Lee, S.A. Vinogradov, C. Sehgal, D.F. Wilson, Oxygen distribution in murine tumors: characterization using oxygen-dependent quenching of phosphorescence. J. Appl. Physiol. (1985) 98(4), 1503–1510 (2005)

    Article  Google Scholar 

  35. J.M. Vanderkooi, G. Maniara, T.J. Green, D.F. Wilson, An optical method for measurement of dioxygen concentration based upon quenching of phosphorescence. J. Biol. Chem. 262(12), 5476–5482 (1987)

    Article  Google Scholar 

  36. X. Cao, S.R. Allu, S. Jiang, M. Jia, J.R. Gunn, C. Yao, E.P. LaRochelle, J.R. Shell, P. Bruza, D.J. Gladstone, L.A. Jarvis, J. Tian, S.A. Vinogradov, B.W. Pogue, Tissue pO2 distributions in xenograft tumors dynamically imaged by Cherenkov-excited phosphorescence during fractionated radiation therapy. Nat. Commun. 11(1), 573 (2020)

    Article  ADS  Google Scholar 

  37. B.W. Pogue, J. Feng, E. LaRochelle, P. Bruza, H. Lin, R. Zhang, J.R. Shell, H. Dehghani, S.C. Davis, S. Vinogradov, D.J. Gladstone, L.A. Jarvis, Maps of in vivo oxygen pressure with submillimetre resolution and nanomolar sensitivity enabled by Cherenkov-excited luminescence scanned imaging. Nat. Biomed. Eng. 2, 254–264 (2018)

    Article  Google Scholar 

  38. H. Lin, R. Zhang, J.R. Gunn, T.V. Esipova, S. Vinogradov, D.J. Gladstone, L.A. Jarvis, B.W. Pogue, Comparison of Cherenkov excited fluorescence and phosphorescence molecular sensing from tissue with external beam irradiation. Phys. Med. Biol. 61(10), 3955–3968 (2016)

    Article  Google Scholar 

  39. R. Zhang, A.V. D’Souza, J.R. Gunn, T.V. Esipova, S.A. Vinogradov, A.K. Glaser, L.A. Jarvis, D.J. Gladstone, B.W. Pogue, Cherenkov-excited luminescence scanned imaging. Opt. Lett. 40(5), 827–830 (2015)

    Article  ADS  Google Scholar 

  40. E. Roussakis, J.A. Spencer, C.P. Lin, S.A. Vinogradov, Two-photon antenna-core oxygen probe with enhanced performance. Anal. Chem. 86(12), 5937–5945 (2014)

    Article  Google Scholar 

  41. B.W. Pogue, R. Zhang, X. Cao, J.M. Jia, A. Petusseau, P. Bruza, S.A. Vinogradov, Review of in vivo optical molecular imaging and sensing from x-ray excitation. J. Biomed. Opt. 26(1), 010902 (2021)

  42. B.W. Pogue, B.C. Wilson, Optical and x-ray technology synergies enabling diagnostic and therapeutic applications in medicine. J. Biomed. Opt. 23(12), 1–17 (2018)

    Article  Google Scholar 

  43. J. Axelsson, A.K. Glaser, D.J. Gladstone, B.W. Pogue, Quantitative Cherenkov emission spectroscopy for tissue oxygenation assessment. Opt. Express. 20(5), 5133–5142 (2012)

    Article  ADS  Google Scholar 

  44. H.H. Ross, Measurement of beta-emitting nuclides using Cerenkov radiation. Anal. Chem. 41(10), 1260–2000 (1969)

    Article  Google Scholar 

  45. A.K. Glaser, R. Zhang, D.J. Gladstone, B.W. Pogue, Optical dosimetry of radiotherapy beams using Cherenkov radiation: the relationship between light emission and dose. Phys. Med. Biol. 59(14), 3789–3811 (2014)

    Article  Google Scholar 

  46. A.K. Glaser, R. Zhang, S.C. Davis, D.J. Gladstone, B.W. Pogue, Time-gated Cherenkov emission spectroscopy from linear accelerator irradiation of tissue phantoms. Opt. Lett. 37(7), 1193–1195 (2012)

    Article  ADS  Google Scholar 

  47. R. Zhang, A.K. Glaser, J. Andreozzi, S. Jiang, L.A. Jarvis, D.J. Gladstone, B.W. Pogue, Beam and tissue factors affecting Cherenkov image intensity for quantitative entrance and exit dosimetry on human tissue. J. Biophotonics 10(5), 645–656 (2017)

    Article  Google Scholar 

  48. A.Y. Lebedev, A.V. Cheprakov, S. Sakadzic, D.A. Boas, D.F. Wilson, S.A. Vinogradov, Dendritic phosphorescent probes for oxygen imaging in biological systems. ACS Appl. Mater. Interfaces 1, 1292–1304 (2009)

    Article  Google Scholar 

  49. S.A. Vinogradov, D.F. Wilson, Porphyrin-dendrimers as biological oxygen sensors, in Designing Dendrimers. ed. by S. Capagna, P. Ceroni (Wiley, New York, 2012)

    Google Scholar 

  50. J. Jansen, J. Knoll, E. Beyreuther, J. Pawelke, R. Skuza, R. Hanley, S. Brons, F. Pagliari, J. Seco, Does FLASH deplete oxygen? Experimental evaluation for photons, protons, and carbon ions. Med. Phys. 48(7), 3982–3990 (2021)

  51. X. Cao, J.R. Gunn, S.R. Allu, P. Bruza, S. Jiang, S.A. Vinogradov, B.W. Pogue, Implantable sensor for local Cherenkov-excited luminescence imaging of tumor pO2 during radiotherapy. J. Biomed. Opt. 25(11), 112704 (2020)

  52. R. Zhang, A.K. Glaser, J. Andreozzi, S. Jiang, L.A. Jarvis, D.J. Gladstone, B.W. Pogue, Beam and tissue factors affecting Cherenkov image intensity for quantitative entrance and exit dosimetry on human tissue. J. Biophotonics 10(5), 645–656 (2016)

    Article  Google Scholar 

  53. K.K. Dwivedi, M.S. Prasad, G.N. Rao, R.K. Dogra, R.K. Upreti, R. Shanker, C.R. Murti, S.S. Kapoor, M. Lal, K.V. Viswanathan, Trace elemental analysis of extracted dust from lungs and lymph nodes of domestic animals using X-ray fluorescence technique. Int. J. Environ. Anal. Chem. 7(3), 205–221 (1980)

    Article  Google Scholar 

  54. J. Borjesson, S. Mattsson, Toxicology; in vivo x-ray fluorescence for the assessment of heavy metal concentrations in man. Appl. Radiat. Isot. 46(6–7), 571–576 (1995)

    Article  Google Scholar 

  55. R. Zhang, L. Li, Y. Sultanbawa, Z.P. Xu, X-ray fluorescence imaging of metals and metalloids in biological systems. Am. J. Nucl. Med. Mol. Imaging 8(3), 169–188 (2018)

    Google Scholar 

  56. K. Langstraat, A. Knijnenberg, G. Edelman, L. van de Merwe, A. van Loon, J. Dik, A. van Asten, Large area imaging of forensic evidence with MA-XRF. Sci. Rep. 7(1), 15056 (2017)

    Article  ADS  Google Scholar 

  57. A. Turyanskaya, M. Rauwolf, V. Pichler, R. Simon, M. Burghammer, O.J.L. Fox, K. Sawhney, J.G. Hofstaetter, A. Roschger, P. Roschger, P. Wobrauschek, C. Streli, Detection and imaging of gadolinium accumulation in human bone tissue by micro- and submicro-XRF. Sci. Rep. 10(1), 6301 (2020)

    Article  ADS  Google Scholar 

  58. G. Pratx, C.M. Carpenter, C. Sun, R.P. Rao, L. Xing, Tomographic molecular imaging of x-ray-excitable nanoparticles. Opt. Lett. 35(20), 3345–3347 (2010)

    Article  ADS  Google Scholar 

  59. C.M. Carpenter, C. Sun, G. Pratx, R. Rao, L. Xing, Hybrid x-ray/optical luminescence imaging: characterization of experimental conditions. Med. Phys. 37(8), 4011–4018 (2010)

    Article  Google Scholar 

  60. W. Cong, Z. Pan, R. Filkins, A. Srivastava, N. Ishaque, P. Stefanov, G. Wang, X-ray micromodulated luminescence tomography in dual-cone geometry. J. Biomed. Opt. 19(7), 076002–076002 (2014)

    Article  ADS  Google Scholar 

  61. D. Chen, S. Zhu, X. Chen, T. Chao, X. Cao, F. Zhao, L. Huang, J. Liang, Quantitative cone beam X-ray luminescence tomography/X-ray computed tomography imaging. Appl. Phys. Lett. 105(19), 191104 (2014)

    Article  ADS  Google Scholar 

  62. X. Liu, Q. Liao, H. Wang, In vivo x-ray luminescence tomographic imaging with single-view data. Opt. Lett. 38(22), 4530–4533 (2013)

    Article  ADS  Google Scholar 

  63. C. Li, K. Di, J. Bec, S.R. Cherry, X-ray luminescence optical tomography imaging: experimental studies. Opt. Lett. 38(13), 2339–2341 (2013)

    Article  ADS  Google Scholar 

  64. C.M. Carpenter, G. Pratx, C. Sun, L. Xing, Limited-angle x-ray luminescence tomography: methodology and feasibility study. Phys. Med. Biol. 56(12), 3487–3502 (2011)

    Article  Google Scholar 

  65. M.C. Lun, W. Zhang, C. Li, Sensitivity study of x-ray luminescence computed tomography. Appl. Opt. 56(11), 3010–3019 (2017)

    Article  ADS  Google Scholar 

  66. D. Chen, F. Meng, F. Zhao, C. Xu, Cone beam X-ray luminescence tomography imaging based on KA-FEM method for small animals. Biomed. Res. Int. 2016, 6450124 (2016)

    Article  Google Scholar 

  67. E.P.M. LaRochelle, J.R. Shell, J.R. Gunn, S.C. Davis, B.W. Pogue, Signal intensity analysis and optimization for in vivo imaging of Cherenkov and excited luminescence. Phys. Med. Biol. 63(8), 085019 (2018)

    Article  Google Scholar 

  68. G. Pratx, C.M. Carpenter, C. Sun, L. Xing, X-ray luminescence computed tomography via selective excitation: a feasibility study. IEEE Trans. Med. Imaging 29(12), 1992–1999 (2010)

    Article  Google Scholar 

  69. M.J. Jia, P. Bruza, L.A. Jarvis, D.J. Gladstone, B.W. Pogue, Multi-beam scan analysis with a clinical LINAC for high resolution Cherenkov-excited molecular luminescence imaging in tissue. Biomed. Opt. Express 9(9), 4217–4234 (2018)

    Article  Google Scholar 

  70. M.J. Jia, X. Cao, J.R. Gunn, P. Bruza, S. Jiang, B.W. Pogue, Tomographic Cherenkov-excited luminescence scanned imaging with multiple pinhole beams recovered via back-projection reconstruction. Opt. Lett. 44(7), 1552–1555 (2019)

    Article  ADS  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge the very useful collaboration and discussions with colleagues related to this work. The support of the National Institutes of Health partially funded this work from R01 EB024498, U24 EB028941 and R21 EB027397.

Funding

This work was funded by the National Institutes of Health grants R01 EB023909, U24 EB028941 and R21 EB027397.

Author information

Authors and Affiliations

  1. Thayer School of Engineering, Dartmouth College, Hanover, NH, USA

    Brian W. Pogue, Xu Cao & Harold M. Swartz

  2. Department of Diagnostic Radiology, Geisel School of Medicine, Dartmouth College, Hanover, NH, USA

    Harold M. Swartz

  3. Department of Biochemistry and Biophysics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA

    Sergei A. Vinogradov

  4. Department of Chemistry, School of Arts and Sciences, University of Pennsylvania, Philadelphia, PA, USA

    Sergei A. Vinogradov

Authors
  1. Brian W. Pogue
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xu Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Harold M. Swartz
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sergei A. Vinogradov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brian W. Pogue.

Ethics declarations

Conflict of interest

Author Brian Pogue declares commercial involvement with DoseOptics LLC, a company developing Cherenkov imaging cameras for radiotherapy dosimetry. Author Sergei Vinogradov declares commercial involvement with Oxygen Enterprises LLC, a company developing oxygen probes for research use.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pogue, B.W., Cao, X., Swartz, H.M. et al. Review of Tissue Oxygenation Sensing During Radiotherapy Based Upon Cherenkov-Excited Luminescence Imaging. Appl Magn Reson 52, 1521–1536 (2021). https://doi.org/10.1007/s00723-021-01400-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00723-021-01400-8

Search

Navigation