Skip to main content
Springer Nature Link
Log in

Going Low in a World Going High: The Physiologic Use of Lower Frequency Electron Paramagnetic Resonance

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

Abstract

Yakov Sergeevich Lebedev was a pioneer in high-frequency EPR, taking advantage of the separation of g-factor anisotropy effects from nuclear hyperfine splitting and the higher-frequency molecular motion sensitivity from higher-frequency measurements (Appl Magn Reson 7: 339–362, 1994). This article celebrates a second EPR subfield in which Prof. Lebedev pioneered, EPR imaging (Chem Phys Lett 99: 301–304, 1983). We celebrate the clinical enhancements that are suggested in this low-frequency work and imaging application to animal physiology at lower-than-standard EPR frequencies.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Abbreviations

EPR:

Electron paramagnetic resonance

O2 :

Molecular oxygen

pO2 :

Partial pressure of dissolved molecular oxygen

MHz:

Megahertz, units of 106 Hz

WWII:

World war two

RF:

Radiofrequency

ρ :

Charge density

J :

Current density

σ :

Material conductivity

E :

Electric field intensity

B :

Magnetic field induction

ω :

Electric and magnetic field temporal angular frequency

ν :

Electric and magnetic field temporal frequency

λ :

Wavelength

k :

Wave number = 2π/λ

ε :

Local material permittivity

μ :

Local material permeability

ESE:

Electron spin echo

SLR:

Spin lattice relaxation

IRESE:

Inversion recovery electron spin echo, a SLR based but echo detected measurement used in pO2 imaging

OX071:

Also known as OX063d24, the spin probe capable of quantitative pO2 imaging

R1e :

Longitudinal electron relaxation rate

R2e :

Transverse electron relaxation rate

T1e :

1/R1e Longitudinal electron relaxation time for signal reduction by 1/e

T2e :

1/R2e Transverse electron relaxation time for signal reduction by 1/e

CW:

Continuous wave (measurement technique)

τ :

Delay time between (1) the 90° pulse rotating magnetization initially oriented in the direction of the tmain magnetic field to a direction transverse to that direction, allowing regions of higher or lower magnetic field to develop larger or smaller phase delays and (2) the 180° pulse rotating the magnetization about the main magnetic field direction to correct for the local magnetic field inhomogeneities leaving only information from intrinsic transverse relaxation processes.

T :

Delay time between (1) the 180° pulse rotating magnetization initially oriented in the direction of the tmain magnetic field to the opposite direction and (2) the 90° pulse rotating magnetization to a direction transverse to that direction, the beginning of a fixed τ electron spin echo magnetization readout

mT:

Millitesla

mT/m:

Millitesla/meter measure of magnetic field gradient strength

TCD:

Tumor control dose

TCDn:

Tumor control fraction n at a particular dose

Gy:

Radiation dose in Joules of energy deposited per Kg material

FSa:

A mouse fibrosarcoma tumor type grown in the progeny of the specific mouse type referred to as C3H that originally developed the fibrosarcoma in response to irritation from repeated application of methylcholanthrine dye

MCa4:

A mammary carcinoma that developed spontaneously in the same mouse type as the FSa fibrosarcoma and grown in the C3H mouse type progeny.

RTOG:

Radiation Therapy Oncology Group, a US national cooperative group organized for the purpose of conducting radiation therapy research and clinical investigations.

XRAD225Cx:

Precision x-ray small animal x-ray radiator and computed tomography machine, North Branford, CT

References

  1. E. Zavoisky, J. Phys. 9, 245 (1945)

    Google Scholar 

  2. Y.S. Lebedev, Appl. Magn. Reson. 7, 339–362 (1994)

    Google Scholar 

  3. E.V. Galtseva, O.Y. Yakimchenko, Y.S. Lebedev, Chem. Phys. Lett. 99, 301–304 (1983)

    ADS  Google Scholar 

  4. P. Roschmann, Med. Phys. 14, 922–931 (1987)

    Google Scholar 

  5. C.C. Johnson, A.W. Guy, Proceedings of the IEEE 60, 692–718 (1972)

    Google Scholar 

  6. H.P. Schwan, K.R. Foster, Proceedings of the IEEE 68, 104–113 (1980)

    Google Scholar 

  7. J.L. Schepps, K.R. Foster, Phys. Med. Biol. 25, 1149–1159 (1980)

    Google Scholar 

  8. J.T. Vaughan, C.J. Snyder, L.J. DelaBarre, P.J. Bolan, J. Tian, L. Bolinger, G. Adriany, P. Andersen, J. Strupp, K. Ugurbil, Magn. Reson. Med. 61, 244–248 (2009)

    Google Scholar 

  9. N. Zhang, X.H. Zhu, E. Yacoub, K. Ugurbil, W. Chen, Exp. Brain Res. 204, 515–524 (2010)

    Google Scholar 

  10. X.X. He, M.A. Erturk, A. Grant, X.P. Wu, R.L. Lagore, L. DelaBarre, Y. Eryaman, G. Adriany, E.J. Van de Auerbach, P.F. Moortele, K. Ugurbil, G.J. Metzger, Magn. Reson. Med. 84, 289–303 (2020)

    Google Scholar 

  11. A. Sadeghi-Tarakameh, L. DelaBarre, R.L. Lagore, A. Torrado-Carvajal, X. Wu, A. Grant, G. Adriany, G.J. Metzger, P.F. Van de Moortele, K. Ugurbil, E. Atalar, Y. Eryaman, Magn. Reson. Med. 84, 484–496 (2020)

    Google Scholar 

  12. H.J. Halpern, M.K. Bowman, in EPR Imaging and in vivo EPR, ed. by G.R. Eaton, S.S. Eaton, K. Ohno (CRC Press, Boca Raton, 1991) Chapt 6

    Google Scholar 

  13. D.I. Hoult, R.E. Richards, J. Magn. Reson. 24, 71–85 (1976)

    ADS  Google Scholar 

  14. G.A. Rinard, R.W. Quine, S.S. Eaton, G.R. Eaton, in Biological Magnetic Resonance, vol. 21, ed. by C. Bender, L.J. Berliner (Kluwer Academic/Plenum Pub. Corp., New York, 2004) pp. 115–154.

  15. G. Schwarz, Munchner Medizinische Wochenschrift 56, 1217–1218 (1909)

    Google Scholar 

  16. R.H. Thomlinson, L.H. Gray, Br. J. Radiol. 9, 539–563 (1955)

    Google Scholar 

  17. M.R. Horsman, A.A. Khalil, M. Nordsmark, C. Grau, J. Overgaard, Radiother. Oncol. 28, 69–71 (1993)

    Google Scholar 

  18. J.M. Henk, P.B. Kunkler, C.W. Smith, Lancet 2, 101–103 (1977)

    Google Scholar 

  19. J.M. Henk, C.W. Smith, Lancet 310, 104–105 (1977)

    Google Scholar 

  20. C.N. Coleman, J.B. Mitchell, J. Clin. Oncol. 17, 1–3 (1999)

    Google Scholar 

  21. M. Hockel, K. Schlenger, S. Hockel, P. Vaupel, Cancer Res. 56, 4509–4515 (1996)

    Google Scholar 

  22. W. Stumm, J.J. Morgan, Aquatic Chemistry: Chemical Equilibria and Rates in Natural Waters, 3rd edn. (Wiley, New York, 1995)

    Google Scholar 

  23. Y.N. Molin, K.M. Salikhov, K.I. Zamaraev, Spin Exchange: Principles and Applications in Chemistry and Biology (Springer, Berlin, 1980)

    Google Scholar 

  24. K.J. Liu, P. Gast, M. Moussavi, S.W. Norby, N. Vahidi, T. Walczak, M. Wu, H.M. Swartz, Proc. Natl. Acad. Sci. USA 90, 5438–5442 (1993)

    ADS  Google Scholar 

  25. G. Ilangovan, A. Manivannan, H. Li, H. Yanagi, J.L. Zweier, P. Kuppusamy, Free Radic. Biol. Med. 32, 139–147 (2002)

    Google Scholar 

  26. B.B. Williams, N. Khan, B. Zaki, A. Hartford, M.S. Ernstoff, H.M. Swartz, Adv. Exp. Med. Biol. 662, 149–156 (2010)

    Google Scholar 

  27. L.J. Berliner (ed.), Spin Labels, vol. 1 (Academic Press, New York, 1976)

    Google Scholar 

  28. J.H. Ardenkjaer-Larsen, A.M. Leach, N. Clarke, J. Urbahn, D. Anderson, T.W. Skloss, J. Magn. Reson. 133, 1–12 (1998)

    ADS  Google Scholar 

  29. C. Mailer, B.H. Robinson, B.B. Williams, H.J. Halpern, Magn. Reson. Med. 49, 1175–1180 (2003)

    Google Scholar 

  30. M. Elas, B.B. Williams, A. Parasca, C. Mailer, C.A. Pelizzari, M.A. Lewis, J.N. River, G.S. Karczmar, E.D. Barth, H.J. Halpern, Magn. Reson. Med. 49, 682–691 (2003)

    Google Scholar 

  31. B. Epel, S.V. Sundramoorthy, E.D. Barth, C. Mailer, H.J. Halpern, Med. Phys. 38, 2045–2052 (2011)

    Google Scholar 

  32. B. Epel, S.V. Sundramoorthy, C. Mailer, H.J. Halpern, Concept Magn. Reson. B. 33B, 163–176 (2008)

    Google Scholar 

  33. B. Epel, M.K. Bowman, C. Mailer, H.J. Halpern, Magn. Reson. Med. 72, 362–368 (2014)

    Google Scholar 

  34. B. Epel, H.J. Halpern, J. Magn. Reson. 254, 56–61 (2015)

    ADS  Google Scholar 

  35. J.M. Backer, V.G. Budker, S.I. Eremenko, Y.N. Molin, Biochim. Biophys. Acta 460, 152–156 (1977)

    Google Scholar 

  36. P.E. Eastman, R.G. Kooser, M.R. Pas, J.H. Freed, J. Chem. Phys. 54, 2690 (1969)

    ADS  Google Scholar 

  37. M.P. Eastman, G.V. Bruno, J.H. Freed, J. Chem. Phys. 52, 2511 (1970)

    ADS  Google Scholar 

  38. P.C. Lauterbur, D.N. Levin, R.B. Marr, J. Magn. Reson. 59, 536–541 (1984)

    ADS  Google Scholar 

  39. M.M. Maltempo, J. Magn. Reson. 69, 156–161 (1986)

    ADS  Google Scholar 

  40. M.M. Maltempo, S.S. Eaton, G.R. Eaton, J. Magn. Reson. 72, 449–455 (1987)

    ADS  Google Scholar 

  41. H.J. Halpern, D.P. Spencer, J. Vanpolen, M.K. Bowman, A.C. Nelson, E.M. Dowey, B.A. Teicher, Rev. Sci. Instrum. 60, 1040–1050 (1989)

    ADS  Google Scholar 

  42. G.A. Rinard, R.W. Ouine, G.R. Eaton, S.S. Eaton, E.D. Barth, C.A. Pelizzari, H.J. Halpern, Concept Magn. Res. 15, 51–58 (2002)

    Google Scholar 

  43. M. Elas, K.H. Ahn, A. Parasca, E.D. Barth, D. Lee, C. Haney, H.J. Halpern, Clin. Cancer Res. 12, 4209–4217 (2006)

    Google Scholar 

  44. G.L. Semenza, Cell 107, 1–3 (2001)

    Google Scholar 

  45. G.L. Semenza, Cancer Metas. Rev. 26, 223–224 (2007)

    Google Scholar 

  46. J. Folkman, E. Merler, C. Abernathy, G. Williams, J. Exp. Med. 133, 275–288 (1971)

    Google Scholar 

  47. M. Elas, D. Hleihel, E.D. Barth, C.R. Haney, K.H. Ahn, C.A. Pelizzari, B. Epel, R.R. Weichselbaum, H.J. Halpern, Mol. Imaging Biol. 13, 1107–1113 (2011)

    Google Scholar 

  48. R. Damadian, Science 171, 1151–1153 (1971)

    ADS  Google Scholar 

  49. R. Damadian, K. Zaner, D. Hor, T. DiMaio, Proc. Natl. Acad. Sci. USA 71, 1471–1473 (1974)

    ADS  Google Scholar 

  50. R. Damadian, K. Zaner, D. Hor, T. DiMaio, L. Minkoff, M. Goldsmith, Ann. NY Acad. Sci. 222, 1048–1076 (1973)

    ADS  Google Scholar 

  51. S. Fridsten, A.C. Hellstrom, K. Hellman, A. Sundin, B. Soderen, L. Blomqvist, Acta Radiol. Open 5, 2058460116679460 (2016)

    Google Scholar 

  52. M. Elas, J.M. Magwood, B. Butler, C. Li, R. Wardak, R. DeVries, E.D. Barth, B. Epel, S. Rubinstein, C.A. Pelizzari, R.R. Weichselbaum, H.J. Halpern, Cancer Res. 73, 5328–5335 (2013)

    Google Scholar 

  53. B. Epel, M.C. Maggio, E.D. Barth, R.C. Miller, C.A. Pelizzari, M. Krzykawska-Serda, S.V. Sundramoorthy, B. Aydogan, R.R. Weichselbaum, V.M. Tormyshev, H.J. Halpern, Int. J. Radiat. Oncol. Biol. Phys. 103, 977–984 (2019)

    Google Scholar 

Download references

Acknowledgements

Funding was provided by National Cancer in Institute (Grant no. R01 CA098575 R01 CA236385) and National Institute of Biomedical Imaging and Bioengineering (Grant nos R01EB029948, P41 EB002034).

Author information

Authors and Affiliations

  1. Center for EPR Imaging in Vivo Physiology, University of Chicago, Chicago, USA

    Howard J. Halpern & Boris M. Epel

  2. Department of Radiation and Cellular Oncology, University of Chicago, Chicago, USA

    Howard J. Halpern & Boris M. Epel

Authors
  1. Howard J. Halpern
    View author publications

    You can also search for this author inPubMed Google Scholar

  2. Boris M. Epel
    View author publications

    You can also search for this author inPubMed Google Scholar

Corresponding author

Correspondence to Howard J. Halpern.

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

Halpern, H.J., Epel, B.M. Going Low in a World Going High: The Physiologic Use of Lower Frequency Electron Paramagnetic Resonance. Appl Magn Reson 51, 887–907 (2020). https://doi.org/10.1007/s00723-020-01261-7

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00723-020-01261-7